Cognitive Evolution From Single Cells To The Human Mind

When Cognitive Evolution first appeared, it immediately became a foundational text for all
cognitive neuroscience researchers. There remains nothing else like it in its scope as it
describes the evolution of the neural systems relevant to cognition from single organisms
to modern humans. The second edition of Cognitive Evolution is an essential read for
anyone who wants to be current in their understanding of cognitive evolution.
Arnold L. Glass, Professor of Psychology, Rutgers University, USA
Rich in detail, engagingly written and nicely illustrated, the book is an excellent resource
for upper-level undergraduates and graduate students in the cognitive sciences. It serves
as a reminder of how even simple cognitive tasks depend on a brain architecture and
circuitry of immense complexity with deep evolutionary roots.
Thurston C. Lacalli, Biology Department, University of Victoria, Canada
Cognitive Evolution
Cognitive Evolution provides an in-depth exploration of the natural history of cognition, from
the beginning of life on Earth to present-day humans. Drawing together evolutionary,
comparative, and neuroscience research, the book brings a unique cognitive perspective to
evolutionary psychology.
The second edition features the latest research and illustrations on emerging topics,
making it a true update of the field. After introducing evolution, Boles adopts an information
processing perspective – from inputs to outputs, with all the mental processes in between to
provide a systematic overview of the evolution of cognition, including its sensory, motoric,
perceptual, and cognitive components. The combination of evolutionary, comparative, and
neuroscience perspectives provides insights on topics like vision, handedness, tools and
planning, spatial perception, pattern recognition, memory, language, and consciousness.
Cognitive Evolution is a comprehensive, essential read for advanced undergraduate and
postgraduate students of cognitive and evolutionary psychology. Researchers will find it a
useful and insightful synthesis of the field, yet even the curious public will find in it much
that is surprising and enlightening.
David B. Boles is Professor Emeritus of Psychology, University of Alabama, Tuscaloosa.

He is a cognitive psychologist who has published widely on brain lateralization and
mental resources. He began reading extensively on comparative and artifact evidence of
cognition as a graduate student, leading to inclusion of evolutionary psychology content
in his subsequent courses. In 2001, he began teaching Comparative and Evolutionary
Approaches to Cognition, a course that transitioned into Cognitive Evolution a few years
later. This book is the product of his extensive, career-long preparations to introduce
students to important evolutionary topics.
Cognitive Evolution
From single cells to the human mind
Second Edition
David B. Boles
Cover image: Getty
Second edition published 2022
by Routledge
605 Third Avenue, New York, NY 10158
and by Routledge
4 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN
Routledge is an imprint of the Taylor & Francis Group, an informa business
© 2022 David B. Boles
The right of David B. Boles to be identified as author of this work has been asserted in
accordance with sections 77 and 78 of the Copyright, Designs and Patents Act 1988.
All rights reserved. No part of this book may be reprinted or reproduced or utilised in any form
or by any electronic, mechanical, or other means, now known or hereafter invented, including
photocopying and recording, or in any information storage or retrieval system, without
permission in writing from the publishers.
Trademark notice: Product or corporate names may be trademarks or registered trademarks, and
are used only for identification and explanation without intent to infringe.
First edition published by Routledge 2019
Library of Congress Cataloguing-in-Publication Data
A catalog record has been requested for this book
ISBN: 978-0-367-68507-2 (hbk)

ISBN: 978-0-367-67955-2 (pbk)
ISBN: 978-1-003-13786-3 (ebk)
DOI: 10.4324/9781003137863
Typeset in Bembo
by MPS Limited, Dehradun
For Joan, Walter, and Madeline.
by Madeline Boles, age 6, published with permission

Contents
Introduction xi
Acknowledgments xiv
SECTION I
Introduction to evolution 1
1 Life begins 3
2 Life gets complicated 17
3 Vertebrates to early mammals 30
4 Later mammals through primates 43
5 Humans 65
SECTION II
Sensation and movement 93
6 The mechanical and chemical senses 95

7 Vision 114
8 The origins of motion 131
9 Bipedalism 144
SECTION III
Perception and cognition 161
10 Praxis and handedness 163

11 Tools and planning 180
12 Spatial perception 206
x Contents
13 Pattern recognition 226
14 Memory 240
15 Language 257
16 Consciousness 279
17 A summary in nine firsts 295
Glossary 304
References 315
Additional picture credits 369
Author index 370
Subject index 376
Introduction
Cognitive Evolution grew out of the needs of instructors and students for a textbook explaining
how we as a species acquired our mental lives. On the one hand, cognitive psychology has
had a rich history of developing descriptions of human mental processes and their
organization, placing them in an information processing framework covering inputs,
outputs, and all the processes in between. On the other hand, evolutionary scientists have
developed a large literature using fossils, artifacts, and comparisons between species to explore
the evolution of such processes. However, for the most part, the two hands have not worked
together to create a cognitive evolution textbook.
When I began teaching an evolutionary psychology course at the University of Alabama in
2001, I noticed the absence of such a textbook among others that took a social approach to
evolutionary psychology. Over the years, it has become clear to me that most evolutionary
courses have covered primarily social materials such as the evolutionary mechanisms relating
to mating, kinship, and competition and cooperation. While there is certainly nothing wrong
with that approach – in fact, it can be quite informative and engaging – it only incorporates a
fraction of the existing knowledge base of evolutionary psychology. A whole world of
cognitive evolution research has not been covered.
Existing in parallel, I came to suspect, was another world of college and university
professors coming from cognitive, perceptual, or neuroscience backgrounds, who might like
to teach an evolutionary psychology course from a different perspective to a universe of
students who could profit from it. In effect, what was needed was a book-length treatment
of “evolutionary cognitive psychology”, recognized by David Buss (2012) as one of several
approaches that together define a unified evolutionary psychology.
Thus, Cognitive Evolution was born, with most chapters of the book debuting in my
classroom in 2007. They have been continuously updated since. This edition cites a number
of references as late as 2021, as up-to-date as possible within the constraints placed by
production. I think readers will find that Cognitive Evolution offers a complete, consistent, and
coherent approach to the evolution of our mental lives that is unmatched by any other
textbook.
Before describing how this book can best be used, I would like to add a bit about its
reception. For several years, I conducted anonymous surveys of my students on a chapter-
wise basis, having a graduate student collect and keep them until grading was complete.
Although most of the survey items (questions) were open-ended, one was a 1-to-7 rating
as to how satisfied the student was with the chapter. Most recently, across the first
16 chapters of the book, the mean rating has been 5.7 and the median 6.0. It has been a
well-received book.
xii Introduction
How to use this book
The book is intended to be used by upper-level undergraduate and graduate students, as
well as by researchers and educators interested in a synthesis of the field. It is organized into
three major sections: Introduction to Evolution, Sensation and Movement, and Perception
and Cognition. Examples of courses in which it could be the primary text include
Evolutionary Psychology, Human Evolutionary Psychology, Evolution of Cognition,
Human Cognitive Evolution, Mind in Evolution, Evolution of Mind and Intelligence, and
Evolution of the Brain.
When I vetted the chapters with colleagues, one biology professor questioned whether it
was really necessary to include the Introduction to Evolution. The answer is an unequivocal
yes. Unlike biology courses, nearly every one of which is permeated by evolutionary
background, most psychology courses have developed for decades with hardly a nod to
evolution. Worse, the state of our public education system, not to mention our religious
education system, is such that in many districts, students receive little or no evolutionary
content. Without the introduction to evolution chapters, many students have insufficient
intellectual background to contend with the misconceptions about evolution that abound in
popular society.
The good news, however, is that the introductory chapters can be covered quickly in the
classroom. I have typically spent only 2 or 2-1/2 weeks to cover all five, and that even
includes a handful of supplementary readings added for good measure. The content is
sufficiently straightforward to allow that.
The second section of the book, on Sensation and Movement, consists of four chapters. In
information processing terms, it covers inputs and outputs, including the mechanical,
chemical, and visual senses, and postural, hand, and leg movements. When covering these
along with supplementary materials, I have allowed 2-1/2 to 3-1/2 weeks.
The real meat of the book, however, is in the seven chapters on Perception and
Cognition. By the time students tackle this material, they understand not only the
principles of evolution, but how information enters the human processing system and is
acted upon. They are fully ready to consider what happens in between. This is the section
that takes best advantage of the explosion of cognitive-related evolution research over the
past 25 years. For that reason, and because of the plethora of supplementary readings that
can be brought to bear, I have typically taken 7 to 7-1/2 weeks to cover this material.
Finally, a 17th chapter summarizes the book’s major findings in nine “firsts”. This requires
only a single session to cover.
Pedagogical mileage will likely vary, particularly with the nature of the course. Having
taught the material as a seminar, I often leave time at the end for student project reports, but
that time could instead be accounted for by interspersing additional supplementary material.
A lecture-based course, on the other hand, will have different needs and different timing.
Although I have not personally done it, I can easily envision developing a more general
lecture course on evolutionary psychology using this textbook supplemented with social
cognition chapters from other sources.
Mileage will also vary with the level of the student. Although the book was written with
upper level undergraduates in mind, I have also used it with PhD-level graduate students
with no complaints or problems. Yet, I have also tried to write it with sufficiently accessible
language that any reasonably well-educated person should be able to use it profitably. I would
be pleased to learn that all who use the book will, to some degree, expand their
understanding of how evolution has guided our thinking and perceiving.
Introduction xiii
I should note that this is a psychology book for those interested in human psychology.
Most of the questions it asks fit under the umbrella of “how did you and I come to
be?” I think that is a reasonable question, and it is assuredly the question that psychology
students with only limited exposure to the topic want answered. However, it is not
shy about taking on comparisons between animal species. Fish, bird, rodent, and
especially primate findings are prominent throughout, illuminating our emergence from
an animal background.
Acknowledgments
I would like to thank my wife, Joan Barth, and children Walter and Madeline for their
unbounded patience and support while I have repeatedly written and revised this text. My
daughter Madeline deserves special recognition for contributing her art.
I would also like to express my appreciation of my late mentor Steve Keele, and of
Mike Posner, Mary Rothbart, and Russell Fernald, then of the University of Oregon, for
supporting the unorthodox collection of major prelim topics that set me on the path
toward writing this book. I also thank the now-forgotten fellow student, a year or two
ahead of me in graduate school (it may have been Tram Neill or Terry Hines), who
convinced me to follow my own star in that endeavor, instead of taking a more orthodox,
“mainstream” cognitive psychology approach. Without that little push, all of this may
never have happened.
I would like to thank a number of Alabama colleagues, both from the university and from
the Geological Survey, who read preliminary drafts of some of the chapters and provided
feedback. They included, in alphabetical order, Fred Andrus, Jim Bindon, Joe Chandler, Fran
Conners, Michael Dillard, David Kopaska-Merkel, Tony Loewald, Ed Merrill, Brad Okdie,
Kelly Pivik, Leslie Rissler, Jason Scofield, Ed Stevenson, Carl Stock, and Emily Wakeman.
I also appreciate the more recent chapter reviews written by Terry Hines and by numerous
anonymous members of my undergraduate and graduate seminars.
Also deserving of thanks are those who helped develop the book for publication. For the
first edition, these included Elena Bellaart, Sophie Crowe, Chris Johnson, Ceri McLardy,
Beverly Peavler, and three anonymous experts who contributed full-book reviews through
Routledge. For the second edition they also include April Peake, Lucy Kennedy, Alex
Howard, Chloe Holland, Salonia Singhania, Helen Evans, and Sumit Kumar.
Finally, I would like to express gratitude to the personnel connected with two resource
repositories. First are the library staff at the University of Alabama. This book was only
made possible by their provision of extensive electronic journal resources covering
virtually every need for a PDF of an article and by their prompt interlibrary loan deliveries
of articles that weren’t available electronically. Second are the staff of Creative Commons,
the online repository of public domain and freely licensable graphics. Just a few years ago,
before their efforts produced explosive growth in useable files, this would have been a
much drabber and less informative book. It goes without saying, of course, that my thanks
extend to the multitude of persons who have made their graphic works available through
the Creative Commons website.
Section I
Introduction to evolution
1 Life begins
No one knows how it started. No one is sure exactly what started. But science is led by
best guesses, and a good guess is that at some point a little over 4 billion years ago, almost a
half billion years after Earth’s formation, a complex molecule became self-replicating.
From that humble, nearly invisible beginning, increased complexity was inevitable due
to descent with modification, acted upon by natural selection. We’ll return to that idea
later to consider it more carefully. First, though, let’s look at the question of how life on
Earth originated.
How did life begin?

One perspective is that life began with self-replicating ribonucleic acid, or RNA – a position
called the “RNA world” hypothesis (Vázques-Salazar & Lazcano, 2018). RNA is composed
of a chain of nucleotides, each composed of a nucleobase (cytosine, guanine, adenine, or uracil,
as shown in Figure 1.1), a sugar, and a phosphate. RNA is similar in structure to deoxyr-
ibonucleic acid, or DNA, the complex molecule that carries our genetic code. RNA is a
simpler molecule, though, both because it is a much shorter chain and because it exists
as a single, rather than double, strand.
RNA is also less stable, liable to alteration by solar radiation or even, over time, by water.
That observation leads some to wonder whether a stabler alternative was the first self-
replicator – perhaps an RNA precursor or a chemical near-relation (Lunine, 2005; Zhang,
Peritz, & Meggers, 2005). Yet even proponents of other molecules usually concede that
life funneled through RNA world at some point.
It has been pointed out that sooner or later, RNA would have required a wrapping to
protect it and to provide a suitable microenvironment for replication. Initially, sheets of
the mineral mica might have served the purpose, with the sheets serving as an incomplete
external barrier that could have nurtured the evolution of a more complete biological one
(Hansma, 2010). Others, however, envision a fatty shell as the initial wrapping (Mallary,
2004). Fancifully, this could have been a bubble generated by a foaming sea that even-
tually became a membrane. In any case, the eventual result would have been a protocell,
a self-replicating compartment enclosing chemical processes.
Early RNA strands were probably short in length, making it doubtful they could
have carried sufficient instructions to execute both protocell activities and self-replication.
The problem may have been solved through a “community” of several RNA strands,
perhaps initially coming together through accident. As a mutually dependent grouping
enclosed in a protocell, this would have been stable, and it could have collectively pro-
vided the required instructional complexity (Szilá gyi, Kö nnyű , & Czá rá n, 2020).
But there is also the problem of metabolism (the cellular process by which energy is made
available). How did a self-replicating molecule harness energy to replicate if it was encased in
DOI: 10.4324/9781003137863-2
4 Introduction to evolution
Figure 1.1 The structure of RNA and DNA.

Source: Difference DNA RNA-EN.svg, CC BY-SA 3.0, Sponk.
a protocell? Somehow chemicals must have traversed the protocell’s membrane, as we will
soon consider.
The beginning of life was a sufficiently complex process that scientific best guesses as to
where and how it originated are incomplete at best. Only recently, after millions of years
of human cognitive evolution, have we had the intellectual tools to identify a range of
possibilities. First, what if life originated…
… In a warm little pond?

In 1871, long before the discovery of RNA and DNA, Charles Darwin suggested that
life originated in a “warm little pond” containing what he thought were the necessary
components of ammonia and phosphorus salts, acted upon by electricity as well as solar
heat and light (Follmann & Brownson, 2009). Modern experiments have varied the in-
gredients to more closely resemble Earth’s primitive chemical composition, and have
been rewarded by the creation of nucleotides, the building blocks necessary to synthesize
RNA. An important condition is that the “pond”, actually a solution in laboratory
glassware, must exist in a reducing atmosphere, meaning an atmosphere with free hy-
drogen and little or no oxygen (Parker et al., 2011). Oxygen interferes with the formation
Life begins 5
of nucleotides because it readily reacts with the simpler carbon-based molecules from
which they are built. Thus, today’s atmosphere, with almost no free hydrogen and
abundant oxygen, would have been quite unsuitable for the creation of life.
Geological evidence tells us, however, that the original primordial atmosphere was in fact
oxygen-free. Earth, formed from rocks attracted by gravity, was ultimately derived from a
parent nebula, but came together during a “heavy bombardment” stage in its early history
(Grimm & Marchi, 2018). A study of the gases that would have been released from such
rocks indicates the creation of an atmosphere rich in hydrogen, methane, ammonia, nitrogen,
and water vapor, but having no free oxygen (Zahnle, Schaefer, & Fegley, 2010). Simulations
suggest it soon reached a stable concentration of 40% hydrogen, a reducing atmosphere
(Saad, 2018).
Eventually, as a light gas, hydrogen was stripped off into space by solar heating and ra-
diation. But that process took time, diminishing only about 2.5 billion years ago (Zahnle,
Catling, & Claire, 2013). Before that, there was a long window of opportunity for an
oxygen-free, reducing atmosphere to generate RNA and cellular life.
The earliest RNA would not necessarily have had the ability to self-replicate. Today’s
RNA generally requires protein to do so, leading to the “chicken-and-egg” problem of
which came first: RNA or protein, each requiring the other for its own reproduction
(Bernhardt, 2012).
However, RNA molecules have been discovered that can split into two components,
each component replicating the other without the aid of proteins (Lincoln & Joyce, 2009;
Robertson & Joyce, 2014). In part because the components are small, replication occurs
relatively efficiently and is self-sustaining. The copies subsequently reassemble into
complete RNA molecules. Importantly, occasional “mutations” occur during replication,
resulting in different variations of the components. Over time, those variations that are
most efficient at replication are found to outcompete the others, resulting in a kind of
evolution where mutations beneficial to self-replication are retained and others are
lost. Natural selection may have operated in a similar way on early RNA components,
producing ever-more-efficient self-replication (Lincoln & Joyce, 2009; Robertson &
Joyce, 2014).
This, or whatever alternative process allowed RNA replication, is thought to have oc-
curred by 3.95 billion years ago, because Canadian rock of that age contains a form of carbon
characteristic of life (Tashiro et al., 2017). It may have occurred even earlier, 4.1 billion years
ago, in that similar carbon has been found in an Australian zircon that old (Bell, Boehnke,
Harrison, & Mao, 2015).
Following the stripping off of light elements, the atmosphere would have been only mildly
reducing, although more so in the immediate vicinity of volcanic vents due to their release of
hydrogen among other gasses (Parker et al., 2011). Eventually, microorganisms evolved that
were capable of photosynthesis, consuming water, and giving off oxygen. That is thought to
have started in bulk no later than 2.6 billion years ago, producing a substantial increase in
atmospheric oxygen by 2.2–2.3 billion years ago (Zahnle et al., 2013). Today’s high 21%
oxygen level was reached about half a billion years ago.
However self-replication originated, an accompanying problem concerns the concentra-
tion of chemical components necessary for reactions to occur. For life to transpire, conditions
had to create RNA in greater abundance than was possible in the thin gruel of a lake or
ocean. Thus, the “warm little pond” of Darwin’s notion, a place where chemicals could
be concentrated through evaporation. Tidal pools are another possibility. Wherever con-
centration occurred, life may have required an assist from a web of chemical reactions
(Box 1.1).
Box 1.1 Cyanide and the origin of life
Did life start with a dose of cyanide? In recent years the favorite poison of
screenwriters has undertaken a new, more productive role, starring in one scenario
for the origin of life.
On early Earth, hydrogen cyanide (HCN) was generated in the reducing
atmosphere, and condensed in water sources such as rain, lakes, and oceans ( Das,
Ghule, & Vanka, 2019). When sufficiently concentrated, as in repeatedly
evaporated pools associated with alkaline lakes ( Toner & Catling, 2019), the
HCN reacted with hydrogen sulfide and ultraviolet light. Given natural variation
between pools in available metals, the result was a web of chemical reactions
capable of producing an impressive array of lipids (fatty or waxy molecules), amino
acids (the building blocks of proteins), and nucleic acids ( Patel, Percivalle, Ritson,
Duffy, & Sutherland, 2015).
All of these components could then have come together when rain caused
overflows, combining the ingredients for the emergence of life ( Service, 2015). For
the most part, its high reactivity with the biological domain having played its role,
cyanide then stepped out of the picture – to achieve fame again with the much later
invention of the murder mystery.
Is this how life began? As in the world of film, a plausible story isn’t necessarily a true
one. Already alternative scripts have emerged, involving cyanide-based chemical
reactions in the atmosphere itself, aided by energy imparted by meteors ( Ferus et al.,
2020), or in meteor impact craters ( Osinski, Cockell, Pontefract, & Sapers, 2020).
If not in a “warm little pond”, could life have begun…
… On clay surfaces?
Another proposal is that chemicals were concentrated on wet clay, which was abundantly
produced by early volcanic activity. Clay’s advantage over ponds and pools is that it not only
concentrates but also scaffolds: That is, it allows molecules to organize on its surface.
Experiments find that volcano-derived clay aids the formation of short chemical chains.
Amino acids, RNA, and proteins bind efficiently to it, especially when the clay carries a
negative charge as it typically does (Ferris, 2005; Zhu et al., 2019). Short RNA chains can
also grow much longer on clay surfaces (Ferris, Joshi, Wang, Miyakawa, & Huang, 2004). In
addition, clay provides protection against reactive chemicals, and it aids RNA self-replication
(Franchi & Gallori, 2005).
Or did life begin…
… Around black smokers?

In 1977, scientists were stunned to discover whole ecosystems organized around “black
smokers” – volcanic vents at the bottom of the sea. Life was thriving there under unim-
aginable pressures and temperatures, the simplest life form being thermophilic (heat-loving)
archaea, a type of single-cell microorganism. Although many species of archaea live in less-
extreme environments, thermophilic types usually require sulfur for growth. They are often
anaerobic (they live without oxygen), and they can exist in isolated locations around local
Life begins 7
black smokers. All these facts suggest that archaea could have evolved in the extreme con-
ditions of Earth’s early history.
It remains to be seen, however, whether the chemistry of black smokers and other
kinds of hydrothermal vents can plausibly have led to RNA. Although high temperatures
may aid the self-assembly of the fatty shell component of protocells ( Jordan et al., 2019),
they impede the folding of RNA into its required three-dimensional structure, and de-
compose both it and its building blocks (Islas, Velasco, Becerra, Delaye, & Lazcano, 2003;
Moulton et al., 2000). Although salt provides some protection against these effects
(Marguet & Forterre, 1998), it is not clear whether salt concentrations were sufficient in
the ancient sea, or whether an early membrane could have enclosed enough salt to allow
high-temperature RNA synthesis.
There is also some evidence against a thermophilic origin of life. The analysis of protein
sequences across life’s domains, including archaea and bacteria, suggests that the earliest-
evolving proteins were temperature sensitive and most likely formed at about 20°C, or 70°F
(Boussau, Blanquart, Necsulea, Lartillot, & Gouy, 2008; Catchpole & Forterre, 2019). That
is more compatible with Darwin’s warm little pond than with the 50–80°C (120–180°F)
temperatures favored by thermophilic organisms. Similarly, the synthesis of amino acids
proceeds best under cold-to-temperate conditions (Cantine & Fournier, 2018).
These results suggest that life originated at relatively low temperatures. However, the
lineages of both archaea and bacteria may have subsequently evolved temperature preferences
in the thermophylic range, before diversifying into both low-temperature and high-
temperature species (Boussau et al., 2008; Catchpole & Forterre, 2019). This scenario has the
potential advantage of permitting low-temperature RNA folding and amino acid synthesis at
the very origin of life, while allowing for later thermophily among both archaea and bacteria.
Or did life emerge…
… In a nuclear geyser system?

A recent proposal, superficially similar to the black smoker proposal but in fact differing
from it in several significant ways, is that life began in a nuclear geyser system. These
involved hot water eruptions on the Earth’s surface, powered by fissioning uranium ore
deep underground.
Today, radioactive decay has depleted natural uranium deposits, making nuclear geysers
things of the distant past. While they operated, however, they offered a number of life-
promoting features. Among them, energy was made available in large quantities, to both
break and form chemical bonds; nutrients and elements were supplied; reducing gas could
have been present in concentrated amounts, especially in caves; and dry-wet cycles existed
to promote the synthesis of RNA. Furthermore, on the Earth’s surface, the high pressure
associated with black smokers was absent. Finally, the environmental features associated
with nuclear geysers were more diverse, making life-forming chemistries more plausible
(Maruyama et al., 2019).
The main drawback of nuclear geysers is that erupted water would have been radioactive,
something that is generally detrimental to life. However, radioactivity-resistant bacteria exist
today, and it is possible that similar resistance was present at life’s outset (Maruyama et al., 2019).
Finally, as a last exercise, did life originate…
… In space?
Reports of organic compounds in meteorites first surfaced in the 19th century, but were
discredited because of contamination due to handling and storage. By the second half of the
20th century, however, sophisticated analyses showed that some uncontaminated meteorites
contain amino acids as well as long-chain hydrocarbons. These molecules are assumed to
have been created by nonbiological processes.
As three-dimensional chemical structures, most amino acids are asymmetric and can exist
equally well in both “left-handed” and “right-handed” forms. Yet on Earth, they are almost
universally left-handed. One advantage of space-based explanations of amino acid creation is
that certain stellar mechanisms can selectively produce left-handedness. Thus, the mind-
boggling possibility exists that a past merging of two neutron stars provided both isotopes and
energy to nearby meteoroids, triggering the formation of predominantly left-handed amino
acids that later found their way to Earth (Famiano, Boyd, Kajino, Onaka, & Mo, 2019).
Although amino acids are not RNA, the formation of complex organic molecules in
extraterrestrial matter allows us to speculate that RNA or its precursors could likewise have
fallen to Earth in meteors, dust grains, or comets. Nucleobases have in fact been found in
meteorites, including uracil, an important component of RNA but not DNA (Pearce &
Pudritz, 2015). Thus, space-originated nucleobases could have helped create RNA world. As
an added bonus, meteorites may have been a major source of phosphate, an important
component in the chemistry of early life (Ritson, Mojzsis, & Sutherland, 2020), and as we
have seen, in the structure of RNA.
Experiments exposing common space materials to radiation like that found in nebulae
have produced a rich array of organic compounds, including amino acids and the full set of
RNA and DNA nucleobases (adenine, cytosine, guanine, thymine, and uracil). The space
materials are powdered meteorites from which organic compounds had been removed, and
formamide, an amide of formic acid. The implication is that important compounds needed to
originate life may have been synthesized in space and then fallen to Earth (Saladino et al.,
2015, 2017).
Even more intriguingly, in 1996, NASA scientists announced fossil evidence of microbial
life in a meteorite discovered 12 years prior on Antarctic ice. The meteorite had presumably
been blasted from the planet Mars by an asteroid impact, for it chemically resembled other
meteorites in which the levels of the inert gases argon, krypton, neon, and xenon matched
concentrations in Mars’ atmosphere (Gibson, McKay, Thomas-Keptra, & Romanek, 2000;
Norton, 1998). The apparent fossils were segmented bodies (Figure 1.2) resembling fossil
bacteria on Earth, but smaller (Gibson et al., 2000).
This extraordinary claim was immediately subjected to intense scientific scrutiny. Some
findings, such as organic material in the meteorite and bacteria-like bodies near its surface,
were found to be attributable to terrestrial contamination. Specifically, the bodies resembled
a bacterium, called Actinomycetales, commonly found in Antarctica (Steele et al., 2000).
Certainly, terrestrial contamination seemed quite possible, since the meteorite had lain in
Antarctica an estimated 13,000 years before its discovery (Gibson et al., 2000).
In a 2008 article, Schulze-Makuch and colleagues reviewed the evidence. They noted that
two other Martian meteorites contain evidence of borehole-like structures, on a microbial
scale, similar to those found in basaltic rocks on Earth, and that the Earth structures test
positive for cellular material. However, terrestrial contamination could still not be ruled out
(Schulze-Makuch, Fairen, & Davila, 2008).
These observations counsel caution in interpreting Martian meteorites, but another ob-
servation is equally important. As others have noted, even if life came from space in cellular
form, that simply pushes the question of life’s origins to an older time and another place. It
seems at least as plausible that life emerged here by building on amino acids and other
complex molecules delivered from space.
So, at the end of the day, how did life emerge? It’s clear from the diverse views just
presented that no one really knows. Certainly, there is no scientific consensus. A diversity of
Life begins 9
Figure 1.2 Evidence for life on Mars? Some have claimed that this 380-nanometer object is a fossilized
bacterium.
Source: ALH84001 structures.jpg, public domain, NASA.
views does not mean that anything is possible, however. Warm little ponds, clay surfaces,
black smokers, nuclear geysers, and space are among a very few possibilities that sensibly
could have sparked life. Possibly, some combination generated it – e.g., with space providing
some of the hydrocarbons that evaporation concentrated in ponds, and with clay or mica
scaffolding the first RNA.
Membranes and metabolism

We’ve considered some possibilities for how life began, but how did it continue to develop?
Let’s approach this question first by thinking about two requirements for life mentioned
earlier: A membrane to protect the organism and to make self-replication possible, and
metabolism to provide the self-replicator with energy.
One of the problems in replicating RNA, as already noted, is that it is easily degraded by
solar radiation and water. While clay or mica surfaces could have played an early protective
role, eventually RNA needed a membrane to protect it from its environment. The mem-
brane could have started as a simple structure based on lipids. Some lipids spontaneously form
bilayers (films) and vesicles (sacs) that can enclose other compounds. Lipid structures also
permit a difference in electrical charge between the inside and outside, a possible precursor of
transport mechanisms that exchange chemicals through living membranes (Trevors, 2003).
Fatty acids, a class of lipids, have been found to form vesicles capable of admitting and
retaining sugars and charged nucleotides. Under certain limited conditions, nucleotides self-
replicate inside the vesicles (Mansy et al., 2008). Pairing a fatty acid vesicle with RNA
benefits both: The vesicle grows better and has greater protection against salt, and the RNA’s
structure is stabilized by its confinement (Saha, Verbanic, & Chen, 2018). Furthermore, it
may not have been a mere accident that a fatty acid membrane formed around RNA. It
appears that as the building blocks of RNA come together, they form stronger bonds to fatty
acids (Xue, Black, Cornell, Drobny, & Keller, 2020). In effect, as RNA formed at the
beginning of life, it may have attracted its own protective membrane.
To survive and reproduce, cells need energy to drive the chemical reactions that build
and maintain structures. Because acidic solutions have abundant hydrogen ions – also
called protons – and those are an energy source, some suggest that early oceans were acidic,
a tongue-in-cheek “primordial vinaigrette” hypothesis (Bernhardt, 2012). Energy may
also have been made available by chemical reactions catalyzed (accelerated) by RNA itself
(Botta, 2004). However, RNA is an inefficient catalyst, so if it served that purpose, it
would soon have been replaced by a more efficient alternative. The role may have been
filled by peptides (short chains of amino acids) admitted through the cell membrane from
the primordial soup (the thin solution of chemicals comprising the early ocean).
Alternatively, peptides may have been manufactured by RNA within the cell, although
that is considered less probable. That is because of the recursion involved – RNA pro-
ducing peptides providing the energy allowing RNA to produce peptides – making it
unlikely to have emerged in a single evolutionary step.
DNA world
Although they had a membrane and a means of metabolism, the first protocells were still
RNA-based. At that point, RNA’s role was one of information storage, its sequences of
nucleobases providing the instructions for manufacturing proteins. But soon, RNA world
gave way to DNA world, with all life thereafter based on the strands of the famous double
helix.
During the transition to DNA world, RNA gave up much of its information storage role
to a molecule that was chemically more stable, less subject to copying errors, and, due to its
length, able to carry instructions for the creation of more complex proteins. The DNA-
protein partnership, combining superior information encoding and superior energy pro-
duction, outcompeted RNA-based life (Lunine, 2005). RNA was, thenceforth, relegated to
a helper role, mediating protein creation based on DNA instructions.
While there is no evidence indicating how RNA gave rise to DNA, an evolutionary
succession is logical because of the similarity of the two molecules. Both have backbones of
phosphate and sugar, and while the sugars differ, they are chemically closely related. To the
backbones of each are attached only four types of nucleobases, and three of the four are
identical between RNA and DNA. It was not a major evolutionary trick to convert RNA or
its chemical precursors into DNA.
Whatever scenario transpired, a period of rapid evolution must have followed in order to
specify the huge number of proteins used subsequently in cell metabolism (Trevors, 2003). At
some point, in some branches of life, light-absorbing pigments were introduced into the cell
as a means of capturing solar energy to drive chemical reactions (Botta, 2004).
One-celled life
Today’s one-celled organisms are either prokaryotes (literally “before kernels” – cells having
no nuclei) or eukaryotes (“true kernels” – cells having nuclei). Based upon similarities and
differences among genes appearing in bacteria, archaea, and eukarya, there is a general
consensus that prokaryotes evolved first (Betts et al., 2018; Boeckmann et al., 2015).
Life begins 11
However, there is no consensus about whether the first cells were bacteria or archaea, the
two prokaryote domains. Some studies favor bacteria (Baldauf et al., 2004; Williams et al.,
2015) and others archaea (Caetano-Anollés et al., 2014; Raymann, Brochier-Armanet, &
Gribaldo, 2015). It may be that there was so much horizontal gene transfer (movement of
genetic material from one organism to another without a parent-child relationship) between
the early domains that a resolution will never be possible based on genes (Thiergart, Landan,
& Martin, 2014). Horizontal gene transfer is also a problem in working out the possible
relationship of viruses to one-celled life (see Box 1.2).
In round figures, prokaryotes are thought to have emerged a little less than 4 billion years
ago, and eukaryotes about 2 billion years ago (Betts et al., 2018; Doglioni, Pignatti, &
Coleman, 2016). The eukaryotes are of particular interest to us because they were ancestral
to animals and then humans.
Box 1.2 Viruses and their relationship to one-celled life
Viruses are noncellular structures ranging from the small and simple to the large
and complex. Their protein shell can surround either a short strand of nucleic acid
(RNA or DNA) encoding one or two proteins, or long strands incorporating over a
thousand genes, some of which are shared by unicellular life ( Figure 1.3).
Figure 1.3 Structure of the tobacco mosaic virus. Some of the protein subunits have been removed to
reveal the coiled RNA.
Source: TMV structure simple.png, CC BY-SA 3.0, Thomas Splettstoesser.
The historical debate over whether viruses are alive, or are instead just chemical
entities, continues even as efforts are made to incorporate them into accounts of the
evolution of life ( Tennant, Fermin, & Foster, 2018). One particularly interesting
attempt was made by Nasir, Kim, and Caetano-Anollés (2017). Recognizing that virus
genes show high rates of both mutation and horizontal gene transfer, they instead
examined a slowly-changing group of proteins. This allowed deep evolutionary
relationships to be explored, based on protein similarities and differences. In
remarkably orderly results, viruses were found to have evolved first, followed
successively by archaea, bacteria, and eukaryotes ( Nasir et al., 2017).
These results call for replication using other approaches, especially since they appear
to resolve not just the relationship of viruses to life’s domains, but the emergence order
of the domains themselves. Yet at minimum, they contribute to increasing recognition
that viruses must be reckoned with when accounting for the early evolution of life
( Tennant et al., 2018).
The eukaryotes, by definition, have nuclei, composed of an inner double membrane
enclosing DNA and proteins. Nuclei thus emerged around 2 billion years ago. It is
thought that another early addition to eukaryotes were mitochondria, small structures re-
sponsible for energy production that exist in multitudes inside today’s cells. Mitochondria
bear a strong resemblance to miniature bacteria and are believed to have initially been
incorporated into eukaryotes in a symbiotic (mutually beneficial) relationship: Mitochondria
provided energy, and eukaryotes provided nutrition and protection (Lane & Martin,
2010). The relationship stuck, and mitochondria became heritable along with the rest of
the cell’s components.
What did the earliest cells look like? It is difficult to be sure, but filaments and strands are
apparent within the first large-scale evidence of life on Earth (Baumgartner et al., 2019).
These are stromatolites – mats of sediment formed by primitive bacteria, dating to 3.5 billion
years ago and found in chert. The mats formed in very shallow water, and similar living
structures can be seen today in the shallow waters of Western Australia (Figure 1.4), the same
place where the fossil ones are found (Cowen, 2005; Westall, 2004).
The earliest stromatolites show no evidence of exposure to oxygen and some evidence
of reduction, suggesting that the microorganisms that created them evolved in a hydrogen-
enriched, reducing atmosphere (Westall, 2004). A likely scenario is that the earliest cells
forming the mats were anaerobic; but, at a later date, such cells emitted oxygen as a by-
product, similar to today’s cyanobacteria. Initially, the oxygen they emitted was scrubbed out
of the atmosphere by dissolved iron in the oceans, which oxidized (rusted) and precipitated
Figure 1.4 Stromatolites in Western Australia.

Source: Stromatolites in Sharkbay.jpg, CC BY-SA 3.0, Paul Harrison.
Life begins 13
out to form ocean floor deposits. Only when oxygen production began to outpace the
weathering-out of iron from rock did oxygen significantly increase in the atmosphere
(Cowen, 2005; Kasting & Catling, 2003; Lunine, 2005).
Remarkably, single-cell organisms were the only life forms on Earth for four-fifths of its
biological history. The first true metazoa, animals in which multiple cells have specialized
roles such as forming body walls, stiffening internal structure, and digestion, appeared only
about 780 million years ago. The long hegemony of the single cell testifies to the difficulties
posed by multicellular organization and to the extensive changes evolution had to create to
make it possible. We turn, next, to a discussion of how evolution works.
The workings of evolution

Even knowledgeable writers sometimes use terminology suggesting that evolution “knows”
where it is going. Such terminology is a shortcut, an easy way to communicate a direction of
change without engaging in a constant struggle to make it clear that no, evolution is not a
conscious thing and therefore accomplishes nothing by premeditation. Even when suggestive
wording is avoided, it is easy for a reader to make the inference anyway. An example might
be the statement that evolution had to create extensive changes to make multicellular life
possible. Although the sentence does not say outright that evolution had a particular di-
rection or intent, it is easy to assume that it did – that it strived toward a “higher”, more
complex organism.
In fact, that is not at all how scientists view the workings of evolution. If evolution
seems to strive toward complexity, it is an illusion arising from the fact that it started with
the simplest possible organism and, by creating change, could only move toward increasing
complexity. There is no reason other than the improbability of the starting point that
evolution could not begin with a highly complex organism and create simplicity. In fact, it
has repeatedly been observed that once evolution created complex organisms, it became
possible for simplification to occur. Thus, vertebrates lost at least nine gene families that
existed in ancestral invertebrates (Danchin, Gouret, & Pontarotti, 2006). In more familiar
examples, ancestral snakes and cavefish respectively lost their legs and eyes (Porter &
Crandall, 2003).
Descent with modification and natural selection

The engine of evolution is nothing more or less than descent with modification, operated upon
by natural selection. Descent with modification means that the genetic instructions of offspring
differ from those of the parents in some way. In sexual organisms, this is accomplished in part
through a reassortment of genetic material, half coming from each parent.
More fundamentally, however, it comes about by imperfect copying. For example, genetic
recombination is an error during the reproduction of chromosomes resulting in the movement
of genetic instructions from one chromosome to another. Or, within a chromosome, there
may be a copying error that results in a slightly altered set of instructions. Such changes,
known as mutations, are often fatal to development; in that case, they are not carried down to
successive generations. Even if a mutation is not fatal, it may involve an inactive portion
of the instructions and have no effect. But, in some cases, a mutation creates a new allele
(alternative form) of an active gene. If the animal carrying the new allele survives, it and the
allele become subject to natural selection.
Natural selection affects the descent of alleles by favoring some over others. Again, there
is no premeditation to this process. Rather, certain capabilities are favored or disfavored by
the environment, and the resulting difference in survival affects transmission to successive
generations. Examples abound, but in keeping with our single-cell theme, consider the
extreme heat around black smokers. This environment favors microbes whose alleles
give them greater heat tolerance over those whose alleles give them less tolerance. The
ability to resist heat is, therefore, likely to be passed to successive generations. Indeed, after
some sufficient number of generations, the descendants become unable to live in a cold
environment.
In black-and-white terms, favored individuals reproduce; unfavored ones die without
reproducing. “Survival of the fittest”, the label used by Herbert Spencer when referring
to Darwin’s (1859) description of natural selection, and later adopted by Darwin himself,
ensures that those organisms best adapted to their environments are more likely to leave
progeny. However, it need not be a black-and-white, live-or-die distinction. For example,
there are and have been only tiny fitness differences between Y chromosomes in the
human population, so that virtually any man has been able to have children. Nevertheless,
all living men descend from the same ancestral Y chromosome that existed on the order of
200,000 years ago (Mendez et al, 2013; Poznik et al., 2013; Scozzari et al., 2014). Thus,
very small fitness differences eliminated all other Y chromosomes over that span of time.
Speciation
Why, then, isn’t there only one species of animal, conqueror of all competitors and supre-
mely fit to rule its environment? The primary reason is that there is no single environment.
At a macro level, water, land, and air make wildly differing demands, and within each, there
are a multitude of niches, each of which favors some animals over others. A koala chewing
Australian gum tree leaves, a gazelle browsing on African grasses, a tiger consuming an Asian
deer, and a grizzly bear feeding on North American salmon have all adapted to particular
environments affording different types of food. Within each of these geographical areas,
countless other species grasp different threads of the web of life.
Speciation, the creation of new species, often occurs due to physical separation between
two parts of an animal population. During the voyage of the ship Beagle, Charles Darwin
collected numerous variations of finches inhabiting different islands of the Galapagos chain
west of South America. The islands provided similar environments, but separation by water
had prevented interbreeding between their inhabitants. Over time, natural selection had
created different variations on different islands. Today, a number of them are considered
separate species.
This kind of speciation is called allopatric, from Greek roots literally meaning “other
native village”. It results in animals well adapted to specific environments and therefore
often “unconquerable” by other species. Allopatric speciation is believed to account for
most of the speciation that has occurred. Besides the water separating islands, geographic
barriers that can divide populations and lead to speciation include mountains, rivers, and
energy-impoverished zones of ocean water such as those separating black smokers from
the surface.
At the other extreme, sympatric (literally “together native village”) speciation occurs in
populations not physically separated. Sympatric speciation can happen if different in-
dividuals in the population feed on differing food sources and mating is linked to those
sources. For example, the apple maggot fly has evolved from a North American fly in-
festing hawthorn fruit. When apple trees were introduced to the continent in the early
19th century, some flies that normally infested hawthorns instead laid their eggs in apples,
probably because of a preexisting geographically related genetic variation that was not
yet a difference between species ( Jiggins & Bridle, 2004). Subsequently, “hawthorn” and
“apple” females showed a preference for mating with males feeding on their preferred
Life begins 15
fruit. This mating preference largely isolated the two groups from one another. Today, the
groups show only low levels of genetic exchange, strongly suggesting the beginnings of
speciation (Feder et al., 1994). Furthermore, a wasp that is parasitic of the flies shows
corresponding change, with apple wasps genetically diverging from hawthorn wasps
(Forbes, Powell, Stelinski, Smith, & Feder, 2009).
A female preference for mating with some males over others is an important aspect of
sexual selection, an adjunct to natural selection. Selection of desirable qualities in mates
makes them more prevalent over successive generations. A classic example is the pre-
ference of many female birds, such as pea hens, for extremes in feather coloration and
form, like those in peacock tails. This is not just a frivolous form of selection, because more
substantial traits often accompany decorative ones. More colorful and robust males tend to
be healthier and better fed, and therefore tend to pass down health-related and possibly
foraging-related traits as well (Boogert, Fawcett, & Lefebvre, 2011).
Is evolution random?
To what extent is evolution a random process? The answer to this depends on which
component of evolution is considered, descent with modification or selection. The
modification part of descent with modification is largely random in that mutations occur at
random places in the genome (the set of genetic instructions embodied in DNA). Although
some of the nucleobases in DNA are more susceptible to change than others, there is no
biochemical equivalent of “pick me!” signaling an intention to change in a particular
direction. Genetic recombinations are also random.
Selection, however, is anything but random. To argue otherwise is to argue, for example,
that fish were equally likely to evolve on land or sea. The truth is that the environment places
strong directional (i.e., nonrandom) demands on organisms. Over time, natural selection,
aided by sexual selection, creates animals that fit their environment, whether it involves the
creation of fin-like structures in both fish and whales, or the creation of wing-like structures
in both birds and bats. Although our ability to predict the specific products of selection is
very limited, general predictions are quite possible. Thus, while no one predicted that
hawthorn maggot flies would like apples, it was inevitable that some North American insect
would come to occupy the new high-energy environmental niche provided by the apple’s
introduction.
Although life began as single cells within a half billion years of Earth’s formation, it took
over 3 billion years more for descent with modification, acted upon by natural selection, to
produce multicellular life. Presumably, speciation played a large role by creating a multitude
of “experiments” that ultimately led to more complex organisms. From that point in history,
we leave the realm of weak evidence and speculation behind, and can rely on a rich fossil
record to trace life’s course. Naturally, we need to accurately date the fossils to reconstruct
the path, and to that topic we soon turn.
Conclusion
Science can only guess at the ultimate origins of life, but an understanding of the natural
processes permitting it is beginning to take shape. A first requirement was replication, a
process implying chemical synthesis involving not only raw materials, but also energy
(metabolism) and a protective envelope (a membrane). The first self-replicating molecule
may have been a short RNA strand formed in a “warm little pond”, on a clay surface,
around a “black smoker”, in a nuclear geyser system, or in space, all representing locations
where energy was available if not abundant. However it originated, the molecule soon
needed a membrane to protect it from the environment, perhaps a bubble based on lipids
that could enclose other compounds.
Although RNA catalyzes a number of chemical reactions, it is not an efficient energy
producer. At some point, RNA was relegated to a support role, with the chemically similar
DNA molecule taking over information coding and, through its coding of proteins, the
production of energy.
The earliest true organisms were prokaryotes, emerging about 4 billion years ago,
although it is unclear whether bacteria or archaea came first. Stromatolites dating
to 3.5 billion years ago, formed in shallow water, record the past presence of primitive
bacteria. Eukaryotes, cells with nuclei, emerged around 2 billion years ago and were the
ancestors of animals including humans. Mitochondria were incorporated into eukaryotes
in the role of energy producer, probably at first in a symbiotic relationship but later in
a heritable one.
The engine of evolution is descent with modification, acted upon by natural selection.
Modification is largely random, involving reassortment and recombination of genetic
material inherited from parents, or mutations occurring to chromosomes prior to or during
copying. Natural selection, however, is driven by environmental characteristics and is
decidedly nonrandom. Even small fitness differences can produce large effects over time,
as in the elimination of all but one ancestral human Y chromosome line within the last
200,000 years or so.
Speciation usually occurs allopatrically, with geographic barriers such as water expanses or
mountains separating two groups, which then evolve independently. However, it may also
occur sympatrically, in the same location, if there are other barriers to interbreeding, such as
differing food preferences. The evolution of complex organisms is the product of countless
genetic “experiments” producing species that could better exploit their environments.
Science stands on far firmer ground with evolution than it does with life’s origins. As we
shall see, evolving life left abundant evidence of descent with modification, acted upon by
natural selection. Some of it would be in the rock around us, and some in every living cell.
2 Life gets complicated
The single-cell aspect of Earth’s earliest life imposed severe limits on the complexity that
could be attained through evolution. Organisms would have to become multicellular for life
to become complicated.
Early sponges were the first true multicellular organisms (called metazoa, or metazoans)
that have left living descendants. Their existence about 650 million years ago is evidenced by
a specific cholesterol-related chemical in rocks of that age from Oman (Gold et al., 2016;
Love et al., 2009). Its principal secretor is a class of sponges called demosponges. The only
other known secretors are algae whose ancestors acquired the characteristic much later, and
therefore cannot account for the earlier deposits (Gold et al., 2016).
As immobile filter feeders, ancestral sponges lacked tissues such as muscles or nervous
systems (Peterson & Butterfield, 2005). However, they possessed specialized cells, including
tubular cells with large pores that allowed water to pass into the animal, and cells with flagella
that pumped it out. Other cells provided structural support through embedded stiff rods
called spicules.
Eumetazoa, the broad group of all animals that are not sponges, are first evidenced by their
apparent effect on acritarchs (tiny acid-resistant fossils showing evidence of a cell wall). Many
acritarchs are believed to have been similar to today’s algae as found in plankton, certainly a
food source for small multicellular animals. Significantly, the form of acritarchs remained
virtually unchanged in the fossil record for hundreds of millions of years – until about
635 million years ago. They then began a rapid evolution of form, with some developing
outward spines, probably as a defense against consumption. The implication seems clear that
eumetazoan consumers had recently evolved, creating a selective pressure for creation of
defensive structures. The dating of these events at 635 million years ago corresponds to
reasonable expectations for the first large populations of motile (independently moving)
metazoans, as opposed to the earlier sessile (attached) sponges. Motility presumably enabled
the consumption of acritarchs (Peterson & Butterfield, 2005).
Unfortunately from a dietary preference alone it is difficult to picture what early eu-
metazoa looked like. Cnidarians (pronounced nigh-dare’-ee-ans), comprised of the jellyfish,
hydras, sea anemones, and related species, are a little more accessible to the imagination.
They first diversified about 605 million years ago(Peterson & Butterfield, 2005), and pre-
sumably originated before that. Like other eumetazoa, they had true tissue serving as skin on
the outside, and a digestive cavity on the inside, the forerunner of the gut (Cowen, 2005;
Steinmetz, Arman, Kraus, & Technau, 2017).
The earliest body fossils of possible eumetazoans date from about 600 million years ago.
Fossils of the genus Vernanimalcula (“small spring animal”) are found in rock known as the
Doushantuo Formation in southwest China. Averaging only 150 micrometers across, they
are bilaterally symmetrical (having mirror-imaged sides) and reportedly have an identifiable
mouth and digestive tract (Petryshyn, Bottjer, Chen, & Gao, 2013). However, these
DOI: 10.4324/9781003137863-3
interpretations are controversial, and Vernanimalcula’s status as a metazoan is not universally
accepted (Cunningham, Vargas, Yin, Bengtson, & Donohue, 2017).
Vernanimalcula is almost exactly 600 million years old. The confident assignment of age is
a key issue in evolutionary science. In this chapter we consider how fossils form, their
dating using geological and molecular clocks, and their role in helping to construct the tree
of life. We also examine the proliferation of species during the Cambrian explosion, in-
cluding the emergence of chordates, which were the ancestors of all vertebrates including
humans.
Fossil formation
A fossil most commonly forms when an organism is covered by sediment, shutting out
oxygen and protecting some parts – most often bones and teeth, but sometimes soft tissues as
well – from rapid decay. Initial burial is followed by a long period in which the parts are
gradually replaced by minerals precipitating from water permeating the sediment. It is not
uncommon, however, for original bones and teeth to survive as fossils. Very rarely, soft
tissues themselves survive without mineralization, as possibly in the cases of preserved tissue
from the dinosaurs Tyrannosaurus rex and Brachylophosaurus canadensis (San Antonio et al.,
2011; Schweitzer et al., 2009). Fossils are usually discovered in sedimentary rocks and vol-
canic ashfalls, and only uncommonly in volcanic lava, which typically consumes organic
material. However and wherever they form, however, fossils are rare and their record should
be assumed incomplete (Box 2.1).
Box 2.1 The fossil record
In a world ideal for paleontologists, all animals would fossilize, and assembling their
record would only involve digging down to the right level in the right place to see
what is there. The discoveries from such a dig, arranged in time, could be likened to a
movie, recording a continuous series of changes in species across time. Unfortunately,
the world is not ideal, and the fossil record more resembles a series of snap-shots than it
does a movie. The snap-shots are widely spaced in time, and the series is almost always
grossly incomplete.
There are many causes of the incomplete fossil record. Most importantly, animals
usually decay without leaving a recognizable trace. It’s not even the case that some
constant percentage of individuals fossilize, because many animals live in environments
disfavoring rapid burial and mineral replacement of body parts. Chimpanzees provide
a good example. Ancestral chimpanzees left almost no fossils, and none of great age,
because most lived in hot, damp forest environments with acidic soils, factors
promoting rapid decay ( McBrearty & Jablonski, 2005; Orwant, 2005).
Nevertheless, an incomplete record can still yield good science. For instance, finding
jawless fishes in older deposits, and jawed fishes in younger ones, suggests that jawed
fishes evolved from jawless ones and not vice versa. Hypotheses formed in this way can
then be tested through new fossil discoveries. If the hypothesis is correct, new fossils
will likely be discovered over time to fill gaps in the record. Yet the approach is
flexible: Should newly discovered fossils prove inconsistent with a hypothesis, it can be
revised or replaced, and tested with future discoveries.
Life gets complicated 19
Geological clocks
Dating a fossil found in rock starts with considering its position on site. A basic consideration is
that rock is generally found in layers, with the oldest on the bottom and the newest on top. Of
course, layers can become inverted from folding of the earth’s crust. Newer rock can also be at
the same level as older rock, as when a river cuts through and deposits sediment, or when
molten rock is injected into sedimentary layers. Careful geological study can identify such cases,
however, and ascertain whether the oldest-on-bottom, newest-on-top relationship holds. But
how do we date the layers? That is the fundamental problem solved by geological clocks.
Assuming undisturbed geology, dating a fossil is straightforward if it is found in rock
sandwiched between layers of volcanic rock or ash. Potassium-argon dating can be used on the
two volcanic layers, and the fossil’s age must then lie between those dates. This method is
possible because minerals forming in a volcanic layer must once have been liquid and
therefore heated enough to drive off any argon gas. However potassium remained behind as a
solid, nongaseous element, with a tiny percentage (about one in 10,000 atoms) existing
naturally in the form of potassium-40, a radioactive isotope. The isotope began decaying over
time into the gas argon-40, becoming trapped in the cooled, solidified material. Thus, by
measuring the existing ratio of potassium-40 to argon-40 and using its known conversion
rate, the age of the volcanic layer can be determined. Because the radioactive half-life of
potasssium-40 is 1.25 billion years, the method is appropriate even for the oldest volcanic
materials on earth (Brown, 1992). However, a number of alternative techniques exist, based
on other radioactive isotopes (for brief, partial reviews, see Brown, 1992, and Levin, 2010).
Dating the Doushantuo Formation in which Vernanimalcula was found proved more
problematic because it is sedimentary, with no closely-spaced volcanic layers allowing precise
“sandwich” dating. Initial attempts to date it used volcanic layers well above and below the
formation, providing a wide range of possible ages, somewhere between 539 and 748 million
years (Barfod et al., 2002).
The problem was eventually solved by determining the age of the sediment itself. When
water deposits certain minerals such as phosphorite, minute quantities of uranium are in-
cluded. The radioactive decay of uranium follows a set sequence producing predictable levels
of lead isotopes. Thus, dating proceeds by measuring the levels of the isotopes. When the
method was applied to Doushantuo phosphorite, the precise age of 599.3 (±4.2) million
years was obtained (Barfod et al., 2002).
Geological clocks are essential tools for dating newly discovered fossil remains. Even when
a rock layer is unsuitable for isotope methods of dating, it is often possible to indirectly derive
a date by identifying ordinary fossil plants and animals within it. If those species have been
dated elsewhere using isotope methods, the date can often be applied to the layer of interest.
Of course, the value of geological clocks increases if more than one method is applied and
the results converge on similar values. But they are not the only dating methods.
Molecular clocks
One of the most exciting developments in late 20th century paleontology was the invention
of molecular clocks. Of great benefit when the fossil record is poor, these estimate when the
ancestors of two species diverged from one another based on quantified differences in DNA.
The forerunners of molecular clocks were clocks based on blood protein differences. These
scored an impressive early victory by showing that primate divergences were much more
recent than most paleontologists assumed (Pilbeam, 1972).
The fundamental assumption of molecular clocks is that genetic differences between
animals are directly related to when they branched off a common ancestor. Closely related
descendants from a common ancestor should show relatively few differences in their genes;
a thousand generations later more differences should be apparent; and a million generations
later differences should be pronounced. This expectation is a direct outcome of the natural
processes that over time damage and miscopy DNA. The fundamental assumption is
therefore so well grounded as to be beyond serious dispute. Instead, the controversial
aspect of molecular clocks is how to calibrate them. In other words, how can genetic
differences be translated into a time scale that can be used to estimate how long ago
species diverged?
The linear molecular clock

The simplest approach to estimating age from molecular differences is to assume a linear
relationship between genetic differences and time. Of course, to arrive at an actual estimate of
the time at which two species diverged, it is necessary to calibrate the clock using fossil record
estimates of one or more divergence times.
Figure 2.1 shows an example from primate ancestry, drawn from early work by Wildman,
Uddin, Liu, Grossman, and Goodman (2003). It uses a 25-million-year-old divergence
between humans and Old World monkeys, and a 14-million-year-old divergence between
humans and orangutans, as inferred from the fossil record.
As these ages predict, and as shown in the figure, Old World monkeys genetically differ from
humans by a greater value (3.76%), than do orangutans (2.18%). The best-fitting line to those
points plus the origin (0% difference at zero million years ago) calibrates the clock, and is then
used to estimate that gorillas, differing from humans by 1.04%, diverged from our ancestral line
6.8 million years ago, and chimps, with a 0.87% difference, 5.6 million years ago.
Of course, these estimates are critically dependent on the calibration points. The ages of
the two used by Wildman and colleagues are now believed to be underestimates, resulting
(as we will see) in somewhat misestimated ages for the gorilla and chimpanzee divergences.
25 Old World monkeys
20
millions of years ago
15
Orangutans
10
Gorillas
5 Chimps
0
0 1 2 3 4
% genetic difference
Figure 2.1 Example of a linear clock using two calibration points (Old World monkeys and orangutans) to
estimate the divergence times of gorillas and chimpanzees from the human ancestral line, based on
genetic differences.
Source: Original figure.
Table 2.1 The major biological taxa, which can be remembered using the
mnemonic “Kings play cards on fat green stools”, as applied to
modern humans. Note that lower levels are members of higher levels,
so, e.g., all primates are also chordates (phylum Chordata)
Kingdom: Animalia (animals)

Phylum: Chordata (animals with a notochord or spinal column)
Class: Mammalia (mammals)
Order: Primates
Family: Hominidae (apes and humans)
Genus: Homo (ancient and modern humans)
Species: sapiens (modern humans)
Calibration aside, comparison to established portions of the primate tree show that a linear
clock provides a fairly good fit to primate data (Drummond, Ho, Phillips, & Rambaut,
2006). That is probably because primate species diverged over a relatively short period of
time, within a single biological order.
More problematic are attempts to extend linear clocks across broad biological taxa (clas-
sifications of organisms based on relatedness; taxon is the singular form) such as a phylum or
kingdom (Table 2.1). Extended across a kingdom, linear clock estimates in excess of one
billion years have been obtained for the common ancestor of all animals (Wang, Kumar, &
Hedges, 1999). Such “deep” estimates are rejected by most scientists because, as we have
seen, the oldest traces of metazoa are only about 650 million years old.
The nonlinear molecular clock

Such deep misestimation of dates by the linear clock means that substantial nonlinearity
must exist when comparing distantly related animals. In other words, the clock must run
fast for some animals and slow for others. Rutschmann (2006) provided a useful listing of
causes of nonlinearity in the molecular clock. One is differences in generation time, the fact
that some species breed at much shorter intervals than others. Over time, the chance that
DNA will be miscopied must be higher for a mouse than for a human, simply because
mice breed far faster and therefore run through many more generations. A second factor is
differences in metabolic rate. Animals with high energy expenditure show faster rates of DNA
synthesis and therefore have more opportunities for miscopying errors. Finally, a third is
differences in DNA repair. To some extent, DNA can repair itself if damaged, and the ability
to do this varies over species (Rutschmann, 2006). As it happens, mice are good examples
of all three factors. Not only do they breed at rapid intervals, they have a high metabolic
rate and they are not as efficient in repairing DNA. No wonder then that mice accrue
genetic errors much more quickly than do humans (Welch & Bromham, 2005), a
straightforward indication that their molecular clock runs fast relative to ours.
The alternative to a linear clock is what has picturesquely been called a “relaxed” or “sloppy”
clock (Rutschmann, 2006). A number of different versions exist, but all share the assumption that
the clock runs at different rates in different branches of the ancestral tree (Welch & Bromham,
2005). Estimation of multiple rates requires considerably more calibration points, so the clock
might more properly be called a “constrained clock” because it stresses the importance of fossil
evidence. Nevertheless, the approach arguably results in a substantially more accurate clock. For
example, a relaxed clock approach using multiple fossil-based anchor points indicated that the
ancestors of chimpanzees and humans diverged 7.5 million years ago (Wilkinson et al., 2011).
Because of the relaxed clock approach and improved calibration, this estimate is believed more
accurate than the 5.6 million-year-old linear clock estimate derived by Wildman et al. (2003).
Do relaxed clock approaches suggest more realistic dates for the metazoan emergence? The
answer is a qualified yes. They certainly shrink the one-billion-plus-years estimate of the
linear clock, but they still produce dates well before any physical evidence of metazoans.
Typically, estimates of about 780 million years are produced, with variability between studies
(e.g., Dohrmann & Wö rheide, 2017; dos Reis, et al., 2015; Peterson, Cotton, Gehling, &
Pisani, 2008). In addition, this age is actually of the first diversification of metazoa into two or
more groups that have left living descendants. The earliest metazoa may have lived well
before they diversified, magnifying the problem (see Box 2.2).
Box 2.2 The two ages of a taxon
By convention, molecular clock studies usually date the age of a taxon as that of its first
diversification into two or more subgroups that have living descendants. Each such
subgroup is called a crown group. However, a taxon’s origin precedes diversification, and
the pre-diversification members are called the stem group. Thus, there are actually two
different ages of a taxon, reflecting the first appearance of crown and stem groups,
respectively ( Renner, 2005).
The two ages bear important implications for which species to compare for molecular
clock purposes. A crown group comparison, the usual type, uses species that are in
different living groups within the taxon. For example, for the African ape taxon
(Homininae), a crown group comparison would be between gorillas and chimpanzees. In
contrast, what might be called a “pre-stem” group comparison pairs a species from the
taxon of interest, with a species from the next earlier taxon that is available along the line
of descent: For example, a comparison between gorillas and orangutans (i.e., non-African
members of the Hominidae). This overestimates the age of the stem group ( Figure 2.2).
Figure 2.2 The crown and stem ages of a taxon. Comparing species marked by the completely or
partially white boxes allows a molecular clock estimate of the crown age. A stem age
comparison, however, is not available because of extinctions. The next best achievable
comparison, between the completely or partially black boxes, is to the next-most-related
species, providing a “pre-stem” age that overestimates the stem age.
A little thought reveals that the true age of a taxon must lie between the dates
yielded by the two comparisons. The “pre-stem” age is an overestimation, but the
crown group age is an underestimation, because the taxon is older than its first
diversification.
The discrepancy with the beginning of physical metazoan evidence 650 million years ago
remains to be explained. Rocks older than that certainly exist, even sedimentary ones, yet
extensive searches have failed to yield unambiguous evidence of metazoan fossils within
them. Initially promising “fossils” of metazoans, and of their relatives the fungi, have been
discounted because they were possibly caused by geological and not biological processes
(Budd & Jensen, 2004; McMahon, 2019). Possibly this is itself part of the problem; if early
metazoan fossils always resemble other things, then unambiguous fossils of the requisite age
may never be identified.
It is also true that fossils are generally younger than an animal’s first appearance, which
likely accounts for at least some of the discrepancy. Metazoan populations would have been
small in the beginning, rendering improbable the preservation and future discovery of their
earliest remains (Budd & Jensen, 2004). Later, as metazoans became abundant, they left a
more extensive and thus more discoverable fossil record. However, it remains to be seen
whether this principle can be stretched sufficiently to cover a gap of 130 million years or so
between the first existence of metazoa and their first physical evidence.
Finally, we should keep in mind that while molecular clocks are valuable, they are only
approximate. Within the bounds of their calibration points, based on uncontroversial
fossils, they appear to yield reasonably accurate estimates of the age of interpolated events.
It is when they are used to extrapolate ancient events outside their calibration points, that
results become controversial. In contrast, geological clocks are usually much more precise,
as exemplified by the dating of the Doushantuo Formation within 4.2 million years.
Nevertheless, both kinds of clocks have their uses. Geological clocks date fossils, while
molecular clocks date the first appearance of new categories of life. Neither substitutes for the
other.
The tree of life

Both kinds of clocks have also proved invaluable in reconstructing the tree of life, a concept
entertained by Charles Darwin. His insight was that all life could be envisioned as a vast tree,
rooted in the distant past and with many branches and twigs extending to the present day.
Before the invention of geological and molecular clocks, the tree of life was reconstructed
by examining anatomical similarities and differences among species, with similar ones as-
sumed to have branched off from a recent common ancestor. This approach is systematized
by cladistics, the grouping of species by novel characteristics absent in less related species. A
clade is a branch on the tree of life defined by one or more characteristic. For example, the
mammalian clade is characterized by fur, which all mammals but no other animals have. Of
course, a clade can be a subset of a larger clade. Artiodactyls are a clade within mammals,
consisting of hooved mammals with an even number of toes (Cowen, 2005).
Characteristics of species are frequently termed either primitive characters or derived characters.
A primitive character is one possessed by the earliest evolving member of a clade. Fur, e.g., is
a primitive character of mammals. A derived character is one possessed by one subgroup but
not all subgroups within a clade. Thus, being hooved with an even number of toes is a
derived character within mammals. Notice that the terms are relative to the clade under
consideration; being hooved with an even number of toes is a primitive character within
artiodactyls.
However, there has sometimes been vigorous debate over the definition of clades. Even
something as intuitively obvious as a mammalian clade can be surprisingly difficult to define,
especially when applied to the fossil record (Cowen, 2005). For present purposes such de-
bates are unimportant, for they are mostly over the labels applied to branches on the tree of
life. The branches themselves are much less controversial.
Today, reconstructing the tree of life is increasingly accomplished by combining cladistics
with analyses of genetic differences between species. Divergences are then dated using sloppy
clocks calibrated with the fossil record.
Figure 2.3 expresses findings using the combined approach, stitched together from a
number of independent research projects. Although it omits date estimates, we can use its
structure to continue exploring the evolution of complex animal life. It certainly captures
much of what has been described thus far. Eukaryotes (eukarya) were among the first groups
to emerge (top left of the figure; note that the bacteria-archaea ordering is controversial),
followed after several branchings by metazoa (middle), which further branched into sponges
and then cnidarians (labels toward the right). Humans emerged many branchings later,
among placental mammals at the very bottom of the figure.
Details of the tree of life are subject to constant revision as additional research accrues. For
example, if archaea are eventually determined to have preceded bacteria, an alteration would
be required to the top part of Figure 2.3. Also, it has been suggested that ctenophores, not
sponges, should be the first metazoans represented (Arcila et al., 2017; Whelan, Kocot,
Moroz, & Halanych, 2015). However, others continue to support the sponges-first depiction
(Nielsen, 2019; Simion et al., 2017).
The Cambrian explosion

An extraordinary feature of the fossil record is that within a short period of 10 to 20 million
years, most of the living metazoan phyla suddenly appeared for the first time. This apparent
rapid evolution of life forms, called the Cambrian explosion, covered all the major branchings
of the tree of life in Figure 2.3 from the Bilateria (bilaterally symmetric animals) through the
Chordata (chordates). Occurring in the narrow range of 520 or 530 to 540 million years ago
(in round figures), it is named for the geological age called the Cambrian Period (in round
figures, 490 to 540 million years ago).
The Cambrian explosion has caused wonder, doubt, and endless theorizing. The wonder,
of course, is that so many animal forms appeared so quickly. As Figure 2.3 indicates, the
branching of the Bilateria down through the chordates includes the ancestral lines of animals
as diverse as insects, clams, starfish, and all vertebrates collectively. That the ancestral lines of
such dissimilar life forms seemingly emerged within 10 to 20 million years is remarkable to
say the least.
Is it a little too remarkable? The Cambrian explosion has had its share of doubters. Early
debate over the explosion concerned the adequacy of the fossil record. Perhaps there had
been previous forms, but they were too soft-bodied to fossilize. If that was the case then
attempting to date the origins of the phyla from fossils would be like trying to reconstruct an
historical event from a photograph taken afterward.
There is no conclusive way to show that the fossil record is adequate, but it is now clear
that sedimentary rocks of the Cambrian and late Precambrian periods exist and do preserve
soft-body evidence. It includes traces of narrow trails 570 million years ago (Collins, Lipps, &
Valentine, 2000; Fedonkin, 2003), and of the so-called “Ediacaran biota”, possibly but not
conclusively animal in nature, extending back 580 million years (Antcliffe, 2012). These
(caption on next page)

Figure 2.3 The eukaryote tree of life, showing some commonly known plant and animal groups. Origin at
top left, progressing to existing phyla on the right. Note that the bracket widths are not meant to
directly reflect time from a common origin.
Source: Copyright © 2004 by Oxford University Press, Inc. Adapted and reproduced with permission of the Licensor
through PLSclear.
demonstrate that soft body parts, and in the case of trails, imprints of soft body parts, did in
fact fossilize. But few are to be found.
What is notable is the lack of hard-body evidence until the 3 to 6 million years immediately
preceding the Cambrian explosion (Shu, Isozaki, Zhang, Han, & Maruyama, 2014;
Valentine, Jablonski, & Erwin, 1999). After that, the proliferation of relatively large animals
with hard-body parts does seem to qualify as an explosion (Butterfield, 2003). If the emerging
phyla became ancestral to most living animals, it is because hard body parts proved exquisitely
adaptable. A skeleton, whether external as in the shells of ancestral insects and crustaceans, or
internal as in sponges or ancestral vertebrates, is invaluable in providing protection from
predators, firm attachment points for muscles, and a framework for repair after damage
(Cowen, 2005).
Early hypotheses on the explosion’s cause cited rising oxygen levels as enabling the
evolution of large, complex bodies. Because oxygen penetrates poorly into external shells,
large-body evolution could not occur until it reached a sufficient concentration that it could
be brought into the body through small openings such as gills (Cowen, 2005). This sup-
position is supported by a correspondence between increasing metazoan consumption of
oxygen, and increasing oxygen levels. Thus, mollusks appeared before arthropods, which
appeared before fishes. Oxygen consumption increased across the three groups, reflecting
atmospheric increases in oxygen (Zhang & Cui, 2016).
It is also possible that hard parts simply took time to evolve, and once they began, were
so successful that hard bodies radiated worldwide. By this account the Cambrian explosion
is self-explanatory. Unfortunately for this explanation, the explosion was not limited
to “hard” animals but also included a proliferation of soft-body forms (Erwin et al., 2011;
Shu et al., 2014).
An ecological view was expressed by Logan, Hayes, Hieshima, and Summons (1995).
They suggested that the earlier proliferation of small metazoans feeding on plankton-like life
forms created a seabed environment that could be exploited by new phyla. Fecal pellets
dropping to the seabed would have created a carpet of high-energy foodstuff while at the
same time improving the oxygenation of the water due to the removal of carbon (which was
therefore not incorporated into carbon dioxide). The strength of this hypothesis is that it
provides one reason why most of the new life forms of the Cambrian explosion had benthic
(bottom-dwelling) lifestyles (Valentine et al., 1999).
Chordates
The Cambrian explosion phylum leading to vertebrates was Chordata, the chordates. These
relatively complex animals have a hollow neural tube behind a notochord (supporting rod)
which stiffens the body and provides muscle attachment points. The neural tube is segmented
into three compartments, namely a forebrain, a hindbrain, and probably a midbrain, the
beginnings of a modular nervous system (Holland & Chen, 2001). A living example thought
to closely model the chordate ancestor is amphioxus (genus Branchiostoma), also known as the
lancelet, a sea-bottom burrowing filter feeder. It is a member of the subphylum cepha-
lochordates. Its importance is its descent from a common ancestor shared by another chordate
subphylum, the vertebrates, but not by other chordate subphyla (Hickman, Roberts, &
Larson, 1997). Thus, its anatomical and behavioral characteristics are important in re-
constructing early vertebrates.
The cephalochordate-vertebrate common ancestor is generally accepted as having evolved
from earlier chordates by neoteny, the retention of juvenile characteristics in adulthood
(Lacalli, 1994). Most invertebrates pass through a larval stage before metamorphosing into
adults. Very often, the larvae swim but the adults are sessile. Thus, assuming it results in a
viable organism, a mutation producing sexual maturity prior to metamorphosis would result
in a swimming, breeding adult, accounting for swimming in the common ancestor.
Amphioxus resembles a translucent fish (sectioned in Figure 2.4), a few centimeters in
length, with no jaw, minimal fins, and with a single eye (Holland & Chen, 2001). Marked
behavioral and structural asymmetries are present despite membership of the chordates in
the Bilateria. As seen from behind, newly hatched amphioxus move by spiraling counter-
clockwise. Among other anatomical asymmetries, the mouth opens on the left and the
mid-gut diverticulum runs along the body’s right side. These asymmetries, and similar ones
in other chordates, indicate that lateral differences, so important to primates as we shall see,
first emerged in chordates’ immediate ancestors, and may be considered a chordate
character (Li et al., 2017). As a result, turning and feeding behaviors in the descendants of
early chordates – i.e., vertebrates – tend to be asymmetric as well, although at least in the
case of fish, different species may show either left or right biases (Stancher, Sovrano, &
Vallortigara, 2020).
By the Cambrian explosion’s end, the chordate phylum was well established. Over
about 250 million years, the animal ancestors of humans had evolved from microscopic
collections of cells to small fishlike creatures. Their neural tubes and anatomical asym-
metries would have important implications for the evolution of sensation, perception, and
cognition. After another 150 million years, some of their descendants would start leaving
the water.
Conclusion
The earliest metazoa are estimated to have emerged about 780 million years ago, although
the first physical evidence in the form of sponge secretions dates to 650 million years ago.
Defense-related changes in the shape of tiny fossil acritarchs 15 million years later suggests a
response to predation, presumably by eumetazoa. After another 30 million years, true tissues
appeared in the cnidarian ancestors of modern jellyfish.
Accurate dating is a key issue in evolutionary science. Geological clocks typically exploit
relative levels of radioactive isotopes to date rock. Molecular clocks use genetic differences
between species to date ancestral divergences. In primates, a linear molecular clock is rea-
sonably accurate. But it breaks down when extended across broad biological taxa, with the
clock found to run at different rates for different animals. Thus, a “relaxed” or “sloppy” clock
is often used, employing fossil evidence to calibrate different branches of the ancestral tree.
Even so controversies emerge, as in the dating of the earliest metazoa. Relaxed clock dates
are only approximate, and decrease in accuracy when used to extrapolate dates outside their
calibration points.
The tree of life is reconstructed using both cladistics (the grouping of species by novel
characteristics), and genetic similarity to map its branches. Its details are constantly revised as
research accrues.
Most living metazoan phyla suddenly appeared during the Cambrian explosion (roughly
520 or 530 to 540 million years ago). Proposed explanations include an inadequate fossil
record preceding the explosion; rising oxygen levels enabling the existence of large, complex
28
Introduction to evolution
Figure 2.4 Section of amphioxus.

Source: Adaptation of Branchiostoma lanceolatum (Amphioxus lanceolatus).png, public domain, Thomas Gyselinck.
bodies; the evolution of hard parts simply taking time but proving highly successful; and the
carpeting of the seabed with fecal pellets that provided high-energy foodstuff for new benthic
(bottom-dwelling) species.
An early branch of animals arising during the explosion and leading to vertebrates was the
chordates, in which a hollow, segmented neural tube accompanies an internal supporting
rod. Amphioxus, a modern species likely similar to the common ancestor of early cepha-
lochordates and vertebrates, resembles a small fish, has a single eye and shows behavioral and
anatomical asymmetries.
3 Vertebrates to early mammals
The evolution of chordates (phylum Chordata) during the Cambrian explosion paved the
way for vertebrates (subphylum Vertebrata), or animals with a brain and a vertebral column
composed of cartilage or bone. In this chapter, we first consider early vertebrates and their
characteristics, before describing the emergence of tetrapods. Their descendants included the
amniotes, as well as the diapsid and synapsid lines of the dinosaurs and mammals.
Early vertebrates
Early vertebrates were fish-like. The Chenjiang rock layers of southern China, dating to
about 520 million years ago, provide one of the most complete fossils of a probable one called
Myllokunmingia fengjiaoa, illustrated in Figure 3.1 (Benton, 2005; Shu et al., 1999). It clearly
shows the presence of upper and lower fins.
Identification of Myllokunmingia as a vertebrate is largely based on evidence of gill pouches as
well as a distinct head with what may have been a cartilaginous skull (Holland & Chen, 2001;
McMenamin, 2019). However, some doubt remains because there is no evidence that the
notochord extended to the head, or that there was a distinct brain. These absences leave open
the possibility that the animal was a prevertebrate craniate (an animal with a skull, in early forms
made of cartilage). Yet either way it must be very close in form to an ancestral vertebrate.
Metaspriggina walcotti, from the Burgess Shale in Canada, likewise had a head, with cranial
cartilage, paired eyes, gill bars, and a notochord. Some identify it as an early vertebrate
(Morris & Caron, 2014) but others as a nonvertebrate chordate (McMenamin, 2019). That it
came from the Walcott Quarry section of the Burgess Shale tightly dates it to 505 million
years ago, give or take a couple of million years (Caron & Rudkin, 2009).
In whatever specific animal a brain first formed, it was a highly significant event, for the
vertebrate brain is what made high-level cognition possible.
Biomineralization
“Harder” evidence of vertebrate status might be taken as biomineralization, the incorporation
of minerals into structures such as bones or teeth. The earliest vertebrates, including those
already described but also the ancestors of hagfish and lampreys, had only cartilage. However,
in quick order dentine (bonelike tissue, but without cells) and true bone emerged, so quickly
in fact that hard parts were an innovation that must have carried a substantial selective ad-
vantage (Keating, Marquart, Marone, & Donoghue, 2018). About 493 million years ago
Anatolepis had primitive teeth, formed from skin that incorporated minerals to form dentine.
That clearly identifies it as a vertebrate, in which both teeth and skin develop from epidermal
cells. Thus, within about 40 million years, natural selection worked from the chordate body
plan to produce identifiable hard parts in early vertebrates (Benton, 2005).
DOI: 10.4324/9781003137863-4
Vertebrates to early mammals 31
Figure 3.1 Fossil of Myllokunmingia fengjiaoa, a probable early vertebrate.

Source: Adaptation of Myllokunmingia big.jpg, CC BY-SA 3.0, Degan Shu, Northwest University, Xi’an, China.
All of these complex animals were sea-dwelling, as evolution had not solved the problems
raised by land habitation. The earliest fossils of land-dwelling, air-breathing animals –
centipedes, millipedes, and arachnids – date back only to about 415 to 425 million years
ago (Rodriguez et al., 2018; Suarez, Brookfield, Catlos, & Stöckli, 2017). Earlier, about
435 millon years ago, arachnids may have gone through a transitional state allowing them to
venture onto land even though they were primarily aquatic (Wendruff, Babcock, Wirkner,
Kluessendorf, & Mikulic, 2020).
By the time of Anatolepis, evolution produced several important adaptations that verte-
brates would build upon. First, the significance of hard parts cannot be overestimated. Teeth
allowed more effective predation, and the later development of bone increased body integrity
while protecting the nervous system and providing a ready supply of calcium (Maisey, 1996).
The notochord, the chordate innovation that supported the neural tube, was incorporated
by vertebrates into the spinal column where both became surrounded by bone. In later-
evolving vertebrates such as reptiles, birds, and mammals, the notochord is most apparent
during embryonic development, transforming to a pulpy mass within the spinal column in
adulthood.
Housed within the spinal column of even the earliest vertebrates was the spinal cord – an
important nervous system innovation, as it served as the conduit for information passing from
peripheral sensors to the brain, and from the brain to the muscles. These would become key
adjuncts to a knowing and acting cognitive brain.
Hox genes
Another major vertebrate adaptation was a multiplication of genes controlling the devel-
opment of body segments, or as has been written, “distinguishing anterior from posterior,
where segments will form in the embryo, where limbs or fins will form, and which way is
up” (Maisey, 1996, p. 31). These Hox genes, an abbreviation of homeobox (i.e., “like a box”,
so named because the DNA sequence is short and can be enclosed by a box in written form)
are believed to have originated no later than the emergence of cnidarians (Ferrier, 2016;
Reddy, Unni, Gungi, Agarwal, & Galande, 2015). In early jellyfish, they may have helped
specify the “bell” at one end, and the mouth and tentacles at the other. Later, during ver-
tebrate evolution, Hox coding was responsible for several innovations including the transi-
tion between fins and limbs, the formation of ribs, and variations in the number of vertebrae
(Pascual-Anaya, D’Aniello, Kuratani, & Garcia-Fernàndez, 2013).
Nonvertebrate chordates have a single cluster of Hox genes, strung like beads on a string
along a single chromosome (or more accurately, because chromosomes are paired, along each
of a single pair of chromosomes). Vertebrates have four clusters, each strung along a different
chromosome. In humans, they are chromosomes 2, 7, 12, and 17 (Hughes, da Silva, &
Friedman, 2001). Within each cluster, a Hox gene’s position determines its influence on a
corresponding body segment. Thus, in each of the four chromosomes involved in verte-
brates, the Hox gene affecting head development is at one end, while the other end has genes
affecting the body’s hind parts (Hickman et al., 1997).
Having four vertebrate clusters instead of one allowed for increased structural complexity
because it permitted more elaborate developmental instructions for different body segments.
One way to quadruple the clusters would have been for the entire genome to double not just
once but twice, a “two-round” theory of genome duplication. Thus, a single cluster on one
chromosome would have become four clusters on different chromosomes (Cañestro, Albalat,
Irimia, & Garcia-Fernàndez, 2013).
Although the two-round theory has had its skeptics (Pervaiz et al., 2019), recent genetic
analysis has strongly supported it. Thus, Simakov et al. (2020) identified 17 ancient chro-
mosomal units shared by widespread animal groups, among others scallops, amphioxus (the
model chordate), and vertebrates (e.g., lampreys, garfish, and chickens). Tracking duplica-
tions across the groups identified two whole-genome duplications in our ancestral line: One
about 490 million years ago, before the emergence of jawed vertebrates, and the other
roughly 450 million years ago, before the emergence of bony fish. However Hox genes
multiplied, mutation followed by natural selection would have caused divergence among the
duplicates, allowing a corresponding increase in the complexity of body structure.
A related vertebrate innovation was the appearance of a neural crest during development,
regulated by Hox genes. In the embryo, the crest consists of a cluster of cells arranged in
ridge-like formations to the sides of the neural tube. Cells from it migrate to various parts of
the body during development to form the brain and many of the nerves and ganglia (func-
tional groupings of nerve cells) – as well as skull bones, teeth, connective tissue, smooth
muscles, and the heart among other organs and tissues (Trainor, Melton, & Manzanares,
2003). The result is a more complex design, including a more complex nervous system to
serve a more complex body plan.
Visual system changes

Particularly important among vertebrate adaptations were changes to the visual system.
Unlike earlier-evolving animals, vertebrates have muscles outside the eye allowing its re-
positioning. The eye also has a small spot of acute central vision called a macula. Eyes occur in
pairs, although this adaptation appeared independently in many invertebrates as well (Rowe,
2004). These characteristics improve vision in multiple ways, by permitting more rapid image
acquisition (i.e., by eye movements instead of whole body movements), by increasing image
resolution (i.e., by way of a macula), and by increasing the size of the visual field (i.e., with
the two eyes pointing in different directions in most vertebrates). Improved vision in turn
called for an increase in the size and complexity of visual processing areas in the brain,
eventually leading to advances in visual cognition including improved object recognition.
Gill arches as predecessors to jaws
Another early vertebrate found in Chenjiang rock was Haikouichthys. Unlike Myllokunmingia,
it possessed clear gill arches, thin support structures for the gills made of cartilage (or bone in
later fishes). Gill arches were a significant development in vertebrates, because jaws are
believed to have evolved through their modification. Specifically, the most anterior (forward)
gill arch developed a joint permitting the mouth to be opened wider. That allowed more
water to be pumped through the gills, thus providing greater oxygenation. The joint in turn
became the basis for evolving a jaw. Thus, jawless fishes first evolved, followed by jawed
fishes perhaps 445 million years ago (Brazeau & Friedman, 2015; Schilling, 2003).
Tetrapods
In 2004, a crew member on a paleontological expedition to the Canadian Arctic found a
snout sticking out of a cliff. It was Tiktaalik, an animal with thick, fleshy, almost hand-like
fins (Figure 3.2). Although not classified among tetrapods – vertebrates with four feet or legs –
it seemed a likely near ancestor of them. Remarkably, the expedition had been mounted to
discover just such a creature. The search, begun five years earlier, ended with the excavation
of three nearly complete fossils, the largest almost nine feet in length (Morelle, 2006).
Scientists had long known that such an animal must have existed. Previously discovered
fossils of Panderichthys (Figure 3.3), dating to 385 million years ago, revealed a creature with
bony gill covers that facilitated the flow of water, indicating a predominantly aquatic lifestyle.
In effect it was a predatory fish. It was lobe-finned, and from such fleshy structures “hands” –
including our own – are believed to have evolved (Ahlberg & Clack, 2006). In comparison,
Acanthostega (365 million years ago) lacked bony gill covers though it retained internal gills,
indicating less water flow and implying that the animal breathed partially out of the water.
This conclusion matches the limb structure, in which the limbs were broad and flat, suitable
Figure 3.2 A reconstruction of Tiktaalik.

Source: Tiktaalik roseae life restor.jpg, public domain, Zina Deretsky, National Science Foundation.
Figure 3.3 The transition from fish (bottom left) to tetrapods (upper right), with Tiktaalik in a transitional
role. A lobe-finned coelacanth fish is also shown for comparison.
Source: Fishapods.png, CC BY-SA 4.0, dave souza.
for propping up the head in shallow water. Eight digits per limb are clearly visible (Laurin,
Girondot, & de Ricqlès, 2000; Shubin, Daeschler, & Coates, 2004). With the earlier animal
finned and the later one not, there must have been a transition between the two forms: A
“predicted Tiktaalik” that was searched for, found, and subsequently described (Daeschler,
Shubin, & Jenkins, 2006).
At 375 million years old, Tiktaalik is a transitional form between fish and tetrapods.
Traditionally, tetrapod evolution was attributed to a shift from water to land, but modern
research points to an intermediate phase in which animals propped themselves up with fleshy
fins in shallow water and mud flats. That gave access to the small prey available there, while
providing protection from large, deeper-water predators. The intermediate animals, the
fossils tell us, were still fish even though they were partially air breathing.
Besides prop fins, transitional forms are believed to have had a prominent tail fin used
when free swimming. Unfortunately the tail of Tiktaalik was not preserved in the fossils,
despite the fanciful ones shown in Figures 3.2 and 3.3. Nevertheless a tail fin was later present
on the true tetrapod Acanthostega (365 million years ago). That animal also had separated
digits, although it was still not a permanent land dweller.
The lineage represented by these species was a freshwater one, evolving in and beside lakes
and streams (Ahlberg & Clack, 2006; Shubin, 2008, pp. 40–41). There is little support for the
alternative, that the water-to-land transition was first made by sea-dwelling animals.
Exactly when hands and feet first appeared is not clear, although the existence of Tiktaalik
and Acanthostega seem to constrain their appearance to between 375 and 365 million years
ago. Unfortunately, fossils of the possible tetrapod Parmastega, dated tightly to 372 million
years ago, lack remains of the hands and feet (Beznosov, Clack, Luksevics, Ruta, & Ahlberg,
2019). Arguments for earlier dates (385–395 million years ago) are based on putative tetrapod
trackways, not remains. Unfortunately, in the absence of independent evidence of hand and
foot structure, their interpretation seems very subjective (e.g., Lucas, 2015) and in some
cases, vulnerable to alternative explanations (King, Shubin, Coates, & Hale, 2011).
The early tetrapods were amphibians, living a larval phase in water and an adult phase on
land like tadpoles and frogs do today. The problems involved in the transition to land were
formidable. Besides the obvious one of breathing air, there were also those of supporting the
body without the buoyancy of immersion, moving across land, feeding, and retaining water.
Lobe-finned fishes had a “leg up” in making the transition because their fleshy fins could
serve as both body supports and thrusters.
Other adaptations were useful as well. Early tetrapods were heavily scaled, aiding water
retention (Cowen, 2005), and they may already have been capable of some air breathing.
Among lobe-finned fishes, lungfish as opposed to coelacanths are the closest relatives of
tetrapods, suggesting that tetrapods evolved from something very similar – and lungfish can
breathe some air (Irisarri & Meyer, 2016; Takezaki & Nishihara, 2017). Finally, lobe-finned
fishes could raise their upper jaw and not just lower their lower jaw, a preadaptation (an
evolutionary change later built upon by other changes) for feeding in the shallows up to
water’s edge without scooping up mud (Cowen, 2005).
During the transition prey were initially captured through water suction, the feeding
method favored by most aquatic vertebrates. Obviously, however, this method is useless for
hunting out of water, so biting eventually evolved. We know roughly when this occurred,
because it is visible in the fossil record: The adjoining edges of skull bones show different
strain patterns in sucking versus biting species. Thus, Eusthenopteron (the earliest species in
Figure 3.3) was a sucker, and Acanthostega was a biter (Markey & Marshall, 2007). Tiktaalik
was also a biter, using a sideways snapping motion to capture prey much like modern cro-
codiles (Hohn-Schulte, Preuschoft, Witzel, & Distler-Hoffmann, 2013).
One peculiarity of early tetrapods is that the modern plan of five digits per limb did not
predominate. More common were six, seven, or eight digits per limb (Bradshaw, 1997;
Coates, Jeffery, & Ruta, 2002; Saxena, Towers, & Cooper, 2017), a condition known as
polydactyly (having more than five digits per limb). The five-a-limb plan did not become
fixed in most tetrapods until it became specified by Hox genes (Kherdjemil et al., 2016). As
Bradshaw (1997) pointed out, if the number of digits had not been reduced in the human
ancestral line we might now be counting in base 12 – or 14, or 16! But regardless of their
number, the evolution of digits would eventually have profound implications for the ma-
nipulation of objects, as well as their creation using memory representations, spatial trans-
formations, and other cognitive tools.
Why did tetrapod ancestors begin to venture onto land? The reason is similar to that
famously given by trailblazing mountaineer George Mallory when asked why he wanted to
scale Mount Everest: “Because it’s there”. Land was an environment lacking predators,
unexploited by animals larger than millipedes, and covered with potentially nutritious ve-
getation. It therefore represented an environmental niche – indeed many niches – waiting to
be filled. Venturing onto land had huge value to the first pioneers.
Amniotes
As advanced as tetrapod amphibians otherwise were, they resembled their fish ancestors by
laying eggs in water. The major innovation of their descendants the amniotes was the
development of embryos within a membrane. In egg-laying species the membrane and
associated shell allow gases to be exchanged with the environment but the embryo to
remain hydrated. That permits the eggs to be hatched on land rather than in water
(Cowen, 2005). In fact it appears that the early amniotes were fully terrestrial, having
relatively complex, multichambered lungs for breathing air (Lambertz, Grommes,
Kohlsdorf, & Perry, 2015).
The first-known amniotes date from about 325 million years ago. This estimate is based on
characteristics other than fossilized eggs, which are missing from the record for well over a
hundred million years after amniotes had to have evolved. It is thought that early eggs
fossilized very poorly because they had little or no mineral content (Piñeiro, Ferigolo,
Meneghel, & Laurin, 2012). Thus, the earliest known eggs, from dinosaurs living about
Figure 3.4 Top to bottom: Anapsid (no-holed), Synapsid (one-holed), and Diapsid (two-holed) skulls.
Source: Adaptation of Skull anapsida 1.svg, Skull anapsida 1.png, and Skull diapsida 1.png, CC BY-SA 3.0, Preto(m).
190 million years ago, had calcium-based shells less than 100 micrometers (0.004 inches)
thick (Stein et al., 2019), about the width of the average human hair.
Instead, dating amniote origins depends on finding evidence of other characteristics of
known amniotes. Those include an anapsid skull (a skull lacking openings behind the eyes; see
Figure 3.4) with a narrow snout; vertebrae allowing head swiveling; and upright rather than
sprawling limbs. Based on these and other characteristics, one of the earliest amniotes was
Westlothiana lizziae (Figure 3.5), found in West Lothian, Scotland (Prothero, 2007,
pp. 234–237; Smithson, Carroll, Panchen, & Andrews, 1994). It inhabited a freshwater lake
environment but was terrestrial and dated to about 325 million years ago (van Tuinen &
Hadly, 2004). These were much smaller animals than the early transitional tetrapods. They
resembled small lizards and were an evolutionary step away from amphibians, although they
were not quite reptiles. They were likely cold-blooded and ate small invertebrates including
insects (Oftedal, 2002), using a weak bite to disable their prey (Kemp, 2005).
Figure 3.5 Reconstruction of Westlothiana lizziae, one of the oldest amniotes.

Source: Westlothiana_BW.jpg, CC BY 3.0, Nobu Tamura.
Synapsids and diapsids
In short order (on an evolutionary time scale), the anapsid amniotes gave rise to two tetrapod
groups, differing in the number of openings in the skull behind the eye. Synapsids had one
opening, and originated about 310 million years ago, while diapsids had two openings, and
appeared a little later (see Figure 3.4). Each gave rise to an important group of vertebrates.
Specifically, diapsids gave rise to dinosaurs and synapsids to mammals.
However, the openings carried significance beyond defining groups. First of all, they
lightened the skull, an increasingly important matter as body sizes enlarged. They also
provided attachment points for heavy jaw musculature, allowing a more powerful bite
(Kemp, 2005; Lee, Reeder, Slowinski, & Lawson, 2004). Finally, for the topmost opening of
diapsids specifically, there may have been a vascular function. In modern alligators and
crocodiles it exchanges heat with the environment, cooling the animals when hot and
heating them when cool, operating as an “air conditioner” – although “heat pump” may be
more apt, since heat flows both ways. Similar function may have applied in extinct diapsids,
such as dinosaurs (Holliday, Porter, Vliet, & Witmer, 2019).
For their part, early synapsids gave rise to therapsids, which in turn became the immediate
ancestors of mammals (Figure 3.6). The synapsid single opening in the skull was then lost as
the cheek bones became jaw muscle attachment points. As a result, living mammals lack the
opening, but nevertheless are considered synapsids by descent (Bard, 2017).
Figure 3.6 Amniote, synapsid, and diapsid relationships. Lines reaching fully to the right are living taxa.
After the synapsids split off, the remaining amniotes can be regarded as primitive reptiles of
which the diapsids were only one group – though a spectacularly successful one. Thus, there
were other early reptiles (e.g., parareptiles) with anapsid skulls (Lee et al., 2004). Figure 3.6
illustrates these relationships.
Dinosaurs
Our main narrative concerns synapsids, but brief consideration of the diapsids, and more
particularly the dinosaurs, is in order. As Figure 3.6 indicates, dinosaurs were a relatively late-
emerging group, first appearing about 225 million years ago (Cowen, 2005). In the popular
mind modern crocodiles and alligators are often imagined to be the remnants of the dinosaurs
but are actually part of a group that split from the dinosaurs’ ancestors a few million years
earlier. It is nevertheless correct to refer to them as the dinosaurs’ nearest living relatives. That
claim pales, though, in comparison to the recent discovery of actual living, breathing
dinosaurs. They are called birds.
Discovery of the feathered Archaeopteryx in 1860 gave firm evidence of a transitional form
between earlier dinosaurs and birds (see Figure 3.7). However, it was Thomas Huxley,
Darwin’s early supporter, who made the first systematic argument that birds and dinosaurs are
related (Ibrahim & Kutschera, 2013). Examining the pelvic bones of a dinosaur in 1868, he
quickly concluded that they were birdlike in character. Other similarities were found in
the vertebrae, leg bones, and toes. Huxley (1870) stated:
there can be no doubt that the hind quarters of the Dinosauria wonderfully approached
those of birds in their general structure, and, therefore, that these extinct reptiles were
more closely allied to birds than any which now live.
It wasn’t until the late-20th-century discovery of numerous feathered dinosaurs in China that
a consensus emerged: Birds are not just related to dinosaurs, but descendants of them and
indeed, cladistically one and the same as them (Cracraft et al., 2004). This affinity appeared
to receive striking confirmation when collagen protein sequences were isolated from
Figure 3.7 A recent reconstruction of Archaeopteryx, a 150-million-year-old dinosaur.

Source: Archaeopteryx, CC BY-SA 2.0, Giles Watson.
well-preserved fossils of a 68-million-year-old Tyrannosaurus rex. They were reported to be
similar to those of the common chicken, and unlike those of mammals. Opposite results were
found for sequences derived from a mastodon (160,000–600,000 years old), which more
closely resembled other mammals and not chickens (Asara, Schweitzer, Freimark, Phillips, &
Cantley, 2007). Subsequent analysis comparing the protein sequences to 21 living species
largely reproduced the expected “tree of life” while confirming the relationships between
mastodons and mammals, and between dinosaurs and birds (Organ et al. 2008). The greater
relationships of the dinosaur-derived peptides to birds and the mastodon-derived peptides
to mammals would seem to argue against criticisms that fossil protein sequences might
result from contamination by recent organisms (e.g., Buckley, Warwood, van Dongen,
Kitchener, & Manning, 2017; Liang, Lau, Saitta, Garvin, & Onstott, 2020).
These results were replicated using a leg bone from a second dinosaur species, an 80-
million-year-old duck-billed hadrosaur called Brachylophosaurus canadensis. Molecularly it was
similar to Tyrannosaurus. Both were found closely related to the ostrich, chicken, and other
birds, less so to alligators, and more remotely to other taxa including mammals (Schweitzer
et al., 2009; Schroeter et al., 2017). Successful extractions of collagen protein sequences from
even older bones, namely from the the 190-million-year-old Lufengosaurus, have been
claimed (Lee et al., 2017), but warnings about possible contamination continue to be
sounded (Saitta et al., 2019).
The large meat- and plant-eating dinosaurs beloved of children and familiar to museum-
goers everywhere evolved and radiated over a period of 160 million years. They descended
from small reptiles whose weight was distributed vertically over the rear legs, producing a
bipedal (two-legged) stance (Lee et al., 2004). While many dinosaurs re-evolved a quadrupedal
(four-legged) stance, bipedalism was favored by many of the later theropods (large carnivorous
dinosaurs with short forelimbs and large jaws). They included such well-known forms as
Allosaurus and Tyrannosaurus. Many millions of years later human ancestors would habitually
mimic the dinosaur’s bipedal form of locomotion in a striking example of convergent evolution
(the evolution of similar form or behavior in relatively unrelated species, due to similar
environmental pressures).
The dinosaur age ended in cataclysm 66 million years ago when a six-mile diameter
asteroid impacted the earth, leaving a vastly larger crater in the Yucatán peninsula of
Mexico and neighboring seabed. Unmistakable evidence for the event includes melted
rock inside the crater, of an age corresponding with the dinosaur extinction, as well as a
similarly aged thin global layer of debris containing high levels of the element iridium.
Iridium is rare on Earth but common in meteorites. Associated with the layer are small
glass spheres as well as “shocked” quartz, the results of an extreme pressure pulse. It is clear
the asteroid blasted out an enormous quantity of partially melted rock, the lightest material
dispersing in the atmosphere to fall worldwide as the iridium-rich layer (Cowen, 2005;
Schulte et al., 2010).
The immediate consequences were a formidable tsunami, evidenced as disordered sedi-
ments up the east coast of the United States, and a years-long blockage of sunlight from dust
lingering in the upper atmosphere. In addition the blasted rock was high in sulfur content,
creating acid rain (Gulick et al., 2019; Schulte et al., 2010). A simulation suggests that at-
mospheric sulfates caused global mean temperature to drop a staggering 27°C (49°F) within
three years of the impact. The average air temperature on Earth’s surface was below freezing
for several years (Brugger, Feulner, & Petri, 2017; Gulick et al., 2019).
Even this might not have caused extinction, but in the prototypical model of bad luck, at
the same time gigantic volcanic eruptions were occurring in India. Within a 750,000-year
period straddling the asteroid event, lava and ash covered an area at least the size of
Texas, and perhaps as large as Texas and Alaska combined, to a depth of over 1.5 miles.
The eruptions contributed significantly to atmospheric dust and to increases in poisonous
trace elements (Kemp, 2005; Schoene et al., 2015), including mercury (Meyer et al., 2019).
Together the two events led to the lowering of global temperatures and a massive die-off
of plants. Ocean plankton greatly declined, and about 80% of land plant species disappeared,
at least in North America (Kemp, 2005). The extinction of all large land animals followed.
Much of the remaining debate is over how quickly extinction occurred – within a few
years according to the majority view emphasizing the asteroid impact, but as many as 250,000
years according to the minority view stressing volcanic eruptions and the poisoning of
embryos within their eggshells. Dinosaurs may also have been in decline for 10 million years
or more preceding these events (Sakamoto, Benton, & Venditti, 2016), with species ex-
tinctions increasing. Those losses were seemingly linked to global cooling that had seen
temperatures fall 7–10ºC, or 13–18ºF, even before the main extinction (Condamine, Guinot,
Benton, & Currie, 2021).
In any case many aquatic animals, crocodilians, birds, insects, and other small land-
dwelling creatures survived. With respect to large land dwellers the age of the dinosaurs was
over. The future belonged to mammals.
Early mammals
Mammal-like synapsids evolved at nearly the same time as the dinosaurs, about 225 million
years ago (Oftedal, 2002). Unfortunately, identifying the first true mammal is difficult despite
numerous fossils covering the transition. That is because mammalian characteristics evolved
gradually at varying times, producing a smooth transition with no clearly marked border
between mammal and nonmammal (Sidor & Hopson, 1998).
For example, endothermy (“warm-bloodedness”, the internal generation of heat to maintain
body temperature) probably evolved in mammalian ancestors as early as 250 million years
ago. Certain fossils of the time reveal ribs shaped to accommodate a diaphragm, nasal bones
associated with warming air before it entered the lungs, and the skeletal build of an active
lifestyle, all signs of endothermy. Less clear is the origin of mammary glands and the nursing
of offspring. However, judging from similarities in lactation across monotreme, marsupial,
and placental mammals, the secretion of milk probably derived from their common ancestor
(Oftedal, 2002). If so it may date from about 220 million years ago (Foley, Springer, &
Teeling, 2016).
Other mammalian characteristics, such as the pairing of a large brain relative to body size –
with its implied consequences for cognition – as well as middle ear bones separated from the
jaw, did not appear until 195 million years ago in the tiny two-gram creature Hadrocodium
(Kemp, 2005). For its part fur is first known with certainty from a “halo” around the fossil
skeleton of Megaconus, a mammal-like animal from 165 million years ago (Zhou, Wu,
Martin, & Luo, 2013).
The multiple-character nature of mammals, accompanied by uncertainty over the onset of
specific characters, makes identification of the first mammal difficult if not impossible. In any
case, our ancestral line depended specifically on the emergence of placental mammals, the
eutheria (“true beasts”). These have fetuses that develop with the aid of a fully formed placenta
and are born live, unlike marsupials that develop without a fully formed one and in most
species without a placenta of any kind. Eutherian ancestors branched off from marsupial
mammals perhaps 170 million years ago (Foley et al., 2016).
The earliest known eutherian was Juramaia, a small climbing mammal weighing a little
over half an ounce, from 160 million years ago (Luo, Yuan, Meng, & Ji, 2011). Closely
related was Eomaia from 125 million years ago. Its fossil is extraordinary in preserving a
pronounced fur halo (Figure 3.8) that makes its mammalian nature instantly clear.
Figure 3.8 Eomaia, a 125-million-year-old eutherian from China.

Source: Eomaia.jpg, CC BY 2.0, Zofia Kielan-Jaworowska and JØrn H. Hurum.
Eomaia was probably partly terrestrial (living on the ground) and partly arboreal (living in trees)
and was adapted for grasping and climbing. Of course, as an internal soft tissue, the placenta did
not fossilize; but the animal can be classified based on similarities to living eutheria in dentition
(the form and patterning of teeth), wrist bones, and ankle bones (Ji et al., 2002).
Like Juramaia, Eomaia was very small, weighing just under an ounce (Ji et al., 2002). It is no
accident that it and other early mammals were tiny. Archosaurs (the dinosaurs and their kin)
ruled the large-animal habitats, while smaller lizard-like reptiles dominated the small-animal
niches. But small warm-blooded mammals could and did thrive in the cool of night. Indeed,
environmental pressure from a nocturnal existence encouraged the evolution of both in-
telligence and sharp senses (Cowen, 2005), including improvements in the senses of smell and
hearing, and in whisker-based touch sensitivity (Maor, Dayan, Ferguson-Gow, & Jones,
2017). When large land animals disappeared after the extinction event 66 million years ago,
new niches opened for the survivors.
Conclusion
Vertebrates originated about 520 million years ago as sea-dwelling animals with brains and
mineralized body parts. Teeth allowed more effective predation, and bones increased body
integrity and protected the nervous system. The emergence of Hox genes, aided by two full-
genome duplications, allowed body segmentation and a new avenue for evolutionary change,
in that one segment could undergo modification without affecting others. Another factor
increasing vertebrate complexity was the neural crest, from which cells migrate during de-
velopment to form nerves, bones, smooth muscles, and other localized structures. Other
vertebrate adaptations included external eye muscles, a macula, and eye pairing, all substantial
improvements of vision.
Tetrapods in the form of four-legged amphibians emerged from fresh water over a period
of about 20 million years. They lived a primarily aquatic existence 385 million years ago but
breathed at least partially out of water 365 million years ago. “Hands” evolved from fleshy
lobe fins, initially with six-to-eight digits each, but becoming fixed at five by Hox genes.
Jaws evolved to open upward, allowing feeding at water’s edge without ingesting mud.
Tiktaalik, a transitional form, captured prey with a sideways snapping motion much like
modern crocodiles.
Amniotes appeared by about 325 million years ago. Their major innovation was to lay eggs
incorporating a membrane, which allowed gas exchange while keeping the embryo hydrated.
This permitted eggs to hatch on land so that from this point, many vertebrates could be
terrestrial in lifestyle. The earliest known shelled eggs date only to about 190 million years
ago, and had shells the width of a human hair. Amniote skulls were anapsid, having no holes
behind the eye.
Synapsids and diapsids, creatures with one versus two holes behind the eye, emerged
shortly afterward and were the ancestors of mammals and dinosaurs respectively. Although
dinosaurs were once thought to be extinct, we now know that birds are their living re-
presentatives. The large dinosaurs disappeared in a cataclysmic extinction 66 million years ago
when a six-mile diameter asteroid collided with the earth. Its dust combined with that from
coinciding volcanic eruptions to create a years-long blockage of sunlight and a calamitous
decline in global temperatures. The ensuing die-off of plants doomed large land animals.
Many smaller animals survived, however, including mammals. Identifying the first
mammals is difficult because of their multiple-character nature, but warm-bloodedness and
lactation probably emerged by 250 and 220 million years ago, respectively. The pairing of a
relatively large brain with middle ear bones that had separated from the jaw likely evolved by
195 million years ago. Fur is known from 165 million years ago.
Eutheria or “true beasts” evolved by 160 million years ago. Eutheria have fully formed
placentas and undergo live birth. Like other early mammals the initial ones were tiny, an
ounce or less in weight, but from such slight beginnings would evolve the large mammals of
post-dinosaur earth.
4 Later mammals through primates
The extinction of large land animals 66 million years ago left a vacuum to be filled by
evolution. Smaller animals survived, including among others lizards, salamanders, birds,
insects, and mammals. The increasing size of mammals would prove to be a major theme
of the postextinction period. Yet the event did not cause an explosive diversification.
Relaxed clock models indicate that all of today’s eutherian orders had emerged long before
the large dinosaurs’ demise. Although diversity did increase in the immediate period
afterward (Close et al., 2020; see Box 4.1), some of it was within orders now extinct
(Springer et al., 2017).
Box 4.1 Mammals and their parasites
The demise of nonavian dinosaurs 66 million years ago was followed by a

diversification of mammals, whose species roughly tripled in number soon after the
extinction ( Close et al., 2020). This expansion, widely noted, was accompanied by a
less noticed, simultaneous diversification: Specifically, of lice.
Molecular clock analysis indicates that parasitic lice originated from nonparasitic
ancestors about 100 million years ago. Finding an evolutionary foothold (literally) on
the fur of mammals and the feathers of dinosaurs, and dining on the blood of their
hosts, they were successful enough to split into two major clades about eight million
years later. After another 25 million years, a third clade emerged just prior to the
dinosaur extinction ( Johnson et al., 2018).
But the real acceleration in louse diversification came in the 20 million years after
the extinction. About nine new taxa appeared, three times the previous number, in a
period only a little over half the length. Among them were clades specializing as
parasites of either mammals or birds, but not both.
The implications seem clear. As mammals and birds diversified following the
extinction event, new environmental niches – i.e., new animal hosts – opened up for
parasites. Codiversification occurred, with mammal and bird diversification followed
by that of lice ( Johnson et al., 2018).
Much later, codiversification also occurred in apes. As gorillas, chimpanzees, and
humans speciated, they each acquired lice particular to them. Nor did it end there: As
the lice in turn speciated, so did their associated bacteria ( Allen, Reed, Perotti, & Braig,
2007; Boyd et al., 2017). Thus, the diversification of one group of organisms led to the
diversification of others.
DOI: 10.4324/9781003137863-5
Before the extinction mammals were already a varied class. Their teeth confirm a diversity
of diets across species, with foods varying between insects, meat, fruit, and seeds. But they
were very small, averaging only 150 g or a little over five ounces before the extinction. That
increased within a million years to one kg (2.2 pounds), about seven times heavier than
before (Novacek, 1999).
In this chapter we examine the emergence of primates from this mammalian background,
and their subsequent diversification into today’s taxa. Those include strepsirrhines; tarsiers;
and the large anthropoid group including New World monkeys, Old World monkeys, and
both the lesser apes and great apes. It should be kept in mind as these species are described
that all have undergone evolution since their ancestors diverged from the primate ancestral
tree. As a result, none is a true representation of its earlier ancestors, any more than a
kangaroo resembles early mammals. However, just as it is possible to deduce characteristics
possessed by early mammals from common characteristics among living mammals (e.g., fur
and endothermy), it is often possible to deduce from common characteristics among a group
of related primates, characteristics possessed by their common ancestor.
Early primates
Only in cartoon worlds did cavemen and large dinosaurs coexist. The reality is that they were
separated by tens of millions of years. Primates, however, did overlap the end of the large
dinosaurs. According to relaxed clock models they originated about 74 million years ago,
give or take four million years, with nearly all estimates dating before the dinosaur extinction
(e.g., Dos Reis et al., 2018; Herrera & Dávalos, 2016; Pozzi et al., 2014; Springer et al., 2017;
Tarver et al., 2016; Zhang et al., 2019).
Despite an origin well inside the geological epoch known as the Late Cretaceous, primates
have fossils only dating to just outside that epoch’s boundary with the Paleocene (Table 4.1),
suggesting a slow emergence. The earliest known primate was Purgatorius, from 66 million
years ago (Mantilla et al., 2021; Silcox & López-Torres, 2017). That earlier primates existed is
implied not only by relaxed clock age estimates, but by the fact that the oldest fossils of
Purgatorius date to about 200,000 years after the dinosaur extinction, and represent two
different species. Because primate speciation is believed to take longer than that, the earliest
representatives of Purgatorius must have predated the extinction (Mantilla et al., 2021). It is
possible that fossils of even earlier primates have been collected, but have not been re-
cognized as primates because of their primitive form (Silcox & López-Torres, 2017).
The recent discovery of tarsal (foot) bones from Purgatorius shows that it had mobile,
grasping feet, as expected of an arboreal, primitive primate but unlike primates’ closest re-
latives, the flying lemurs and tree shrews (Chester, Bloch, Boyer, & Clemens, 2015). Its small
Table 4.1 Geological epochs immediately before and following the

dinosaur extinction
Epoch Dates
Late Cretaceous 101-66 million years ago (mya)

Paleocene 66-56 mya
Eocene 56-34 mya
Oligocene 34-23 mya
Miocene 23-5.3 mya
Pliocene 5.3-2.6 mya
Pleistocene 2.6-0.01 mya
Holocene 0.01 mya-present
Later mammals through primates 45
size of 50 g (a little less than two ounces) suggests that it was an omnivore (both animal and
plant eater), obtaining protein from insects but also eating fruit (Silcox & López-Torres,
2017), very much like its closest mammalian relatives (Selig, Sargis, & Silcox, 2019). To an
untrained eye Purgatorius would have been unremarkable, perhaps squirrel-like. Recognizing
that, Chester and colleagues wryly noted that “the divergence of primates from other
mammals was not a dramatic event” (Chester et al., 2015, p. 1491).
Early primates are generally accepted to have been nocturnal (active at night), a lifestyle that
helped them survive alongside dinosaurs even though there were probably nocturnal dinosaurs
(Santini, Rojas, & Donati, 2015; Schmitz & Motani, 2011). Characteristics of today’s primates
include grasping hands and feet with opposable thumbs (ones that can rotate along their long axis,
allowing contact with the other fingers of the same hand), the modification of claws to rela-
tively flat nails; eye convergence toward the front of the face with resulting stereoscopic vision;
and large eyes and brains for a given body size (Rasmussen, 2002b; Silcox & López-Torres,
2017). As we will see, opposable thumbs, stereoscopic vision, and an enlarged brain improved
object manipulation, and then many millions of years later, object creation itself.
Opposability and nails are beautifully represented in a nearly complete skeleton of
Carpolestes simpsoni (Sussman, Rasmussen, & Raven, 2013). This species originated about
58 million years ago. Following the aforementioned list of characters, it too was a primate
(Chester et al., 2015). Figure 4.1 shows an artist’s reconstruction.
This animal’s big toe was curved, indicating opposability, and it had a flattened end
segment accommodating a nail. These were adaptations for grasping branches, probably
because Carpolestes fed at their slender ends as an omnivore though one emphasizing fruit
(Bloch & Wilcox, 2006; Silcox & López-Torres, 2017). Claw loss probably resulted from
their declining effectiveness as clinging devices as body sizes increased. Flattened digits,
substituting nails for claws, were increasingly favored because of their increased gripping
surface (Soligo & Martin, 2006).
The strepsirrhine-haplorhine divergence

An early branching of the primate tree of life led to important consequences today, namely a
split between the suborders of Strepsirrhini (or strepsirrhines, i.e., wet nosed primates) and
Haplorhini (or haplorhines, i.e., dry nosed primates). Following the split, the haplorhines can
be viewed as a “remainder clade” that includes human ancestors. As Figure 4.2 indicates,
Figure 4.1 Carpolestes simpsoni.

Source: CarpolestesCL.png, CC BY-SA 3.0, Sisyphos23.
Figure 4.2 Cladogram illustrating early branching of the primates. Earlier splits are to the lower left; later
ones to the upper right.
Figure 4.3 Ring-tailed lemur.

Source: Lemur catta 001.jpg, CC BY-SA 3.0, Alex Dunkle (Maky).
Figure 4.4 Northern greater galago.

Source: Garnett’s Galago (Greater Bushbaby).jpg, CC BY SA 2.0, Mark Dumont.
lemur-like animals were among the Strepsirrhini, and indeed, these were the ancestors of living
strepsirrhines, among them lemurs (Figure 4.3), sikafas, pottos, and galagos (Figure 4.4).
Strepsirrhines are found in continental Africa, Madagascar and nearby islands, and
southeast Asia. With few exceptions, all species have a dental comb (outward-projecting
lower canines and incisors, used as a comb while grooming), a divided lower jaw with a
joint at the chin (as in most mammals), elongated noses, and a divided upper lip closely
attached to the gums. Many are nocturnal and have a breeding season as opposed to in-
dividual cycles. Across species their food sources include leaves and other vegetation,
insects, and fruit (Cartmill, 1992).
The split of the Strepsirrhini from other primates is thought to have occurred about
68 million years ago (Table 4.2), although their earliest fossils date from several million years
later (Shoshani, Groves, Simons, & Gunnell, 1996). The Eocene yields evidence of about
40 genera of strepsirrhines. By that time there were both nocturnal and diurnal (active in
daytime) species. They moved by leaping and jumping (Simons, 1992), which were probably
inherited from their immediate primate ancestors (Boyer, Toussaint, & Godinot, 2017).
Table 4.2 Approximate dates of primate divergences from the human ancestral line (which follows the
remainder clades). (Derived in part from Perelman et al., 2011; Pozzi et al., 2014; Schrago &
Voloch, 2013; Tarver et al., 2016; and Zhang et al., 2019.)
Divergence Living examples Remainder clade Date
strepsirrhines lemurs, galagos haplorhines 68 mya

tarsiformes tarsiers anthropoids 66 mya
platyrrhines capuchins, howlers catarrhines 44 mya
Old World monkeys macaques, baboons apes 29 mya
lesser apes gibbons, siamangs great apes 20 mya
orangutans Bornean, Sumatran African apes 15 mya
gorillas eastern, western chimps/humans 9 mya
chimpanzees common chimp, bonobo humans 7.5 mya
The tarsier-anthropoid divergence
The splitting off of the line leading to tarsiers (Figures 4.2 and 4.5) occurred about 66 million
years ago (Table 4.2), leaving the remainder clade Anthropoidea (or anthropoids, i.e., mon-
keys, apes, and man). Together with the Strepsirrhini, tarsiers have traditionally been called
prosimians (“before monkeys and apes”), a grouping losing favor as it has become clear that
tarsiers are both dry-nosed and genetically less similar to the Strepsirrhini than they are to
anthropoids (Pozzi et al., 2014; Shoshani et al., 1996). Nocturnal, clinging insectivores (insect
eaters), tarsiers live on islands in southeast Asia.
The best known of the early Anthropoidea are two species of the genus Eosimias
(Figure 4.6). These appeared by mid-Eocene, about 45 million years ago. Most of their fossils
are in the form of jaws, teeth, and foot bones. From these it is known they were better
adapted than strepsirrhines for horizontal body postures. Nevertheless their big toe was a
grasping one, and therefore more similar to tarsiers than to living anthropoids. Eosimias was
still well under half a pound in weight (Gebo, Dagosto, Beard, Qi, & Wang, 2000; Gebo,
Beard, Ni, & Dagosto, 2015).
As seen in living examples, anthropoid adaptations include more convergent eyes, pre-
sumably for improved depth perception; a shift toward a diurnal lifestyle (Ross, 2000); and a
fully fused chin joint.
The platyrrhine-catarrhine divergence

A particularly important split involving descendants of the early anthropoids, was of
the Platyrrhini (“broad-nosed” monkeys) from the Catarrhini (“narrow-nosed” monkeys).
The platyrrhines are known as New World monkeys (i.e., living in the Americas). Conversely,
the catarrhines are the Old World monkeys (i.e., living in Africa, Asia, and Europe) as well as
the apes including humans. The platyrrhine-catarrhine divergence was about 44 million years
ago (Table 4.2).
Figure 4.5 Tarsier.

Source: Tarsier Sanctuary, Corella, Bohol (2052878890).jpg, CC BY 2.0, yeowatzup.
Figure 4.6 Artist’s conception of Eosimias.

Source: EosimiasDB15.jpg, CC BY-SA 4.0, DiBgd.
New World monkeys

Although our focus is mostly on the Old World lineage as ancestral to humans, it is worth
spending a bit of time on New World monkeys. How they wound up in South America is one of
the great mysteries of primate evolution. The order of primates evolved in the Old World, and no
fossil primates are known from South America before the divergence or even for several million
years afterward. Accordingly it is assumed they arrived there from elsewhere (Dagosto, 2002).
But from where? Any answer must be consistent with two observations stemming from
the movement of the earth’s tectonic plates. First, 44 million years ago there were multiple
interruptions in the Central American land bridge between North and South America.
Second, while closer than it is at present, Africa was nevertheless 1,300 km (800 miles) away
from South America (de Oliveira, Molina, & Marroig, 2009; Houle, 1999).
These considerations pose problems for all three of the hypotheses that might account for
the existence of South American monkeys. These are that they arrived by migration from (a)
North America, (b) Asia, or (c) Africa. The least geographically extreme possibility is that
they came from North America, but the multiple gaps in the land bridge were a significant
barrier. Worse yet, platyrrhines were anthropoids, and no anthropoids are known from
North America at that time.
The second possibility, that they were from Asia, has exactly the same problems: They
would have had to be present in North America, where no anthropoid fossils of the time are
known, and then traverse the broken land bridge. But, in addition, they would first have had
to cross the Bering Strait between Asia and America (Dagosto, 2002).
By a process of elimination that leaves an African origin. But is it really possible that they
came across the Atlantic from Africa? At present this is actually the favored hypothesis
(Dagosto, 2002; de Oliveira et al., 2009). It is supported in part by anatomical similarities
between platyrrhines and African anthropoids (Schrago & Russo, 2003).
However, before we imagine a troop of African monkeys planning a westward adventure
and busily building rafts from woven vines and branches, it’s important to understand just
what is proposed. The migration would have been entirely accidental, with a very small
number of monkeys surviving the journey on a mat of vegetation – a “floating island” – swept
down a river and then offshore by a storm, and carried across by wind and current (Schrago &
Russo, 2003). One such island, observed on a Canadian river in 1881, measured 60 by 23 m
(200 by 75 ft), and was only a piece of what had been a larger floating island. The piece
reportedly had upright trees reaching 15 m (50 ft) in height (Houle, 1999).
While our first reaction to the possibility of a land animal migration across large expanses of
ocean may be to consider it “improbable, unobservable and consequently untenable” (Censky,
Hodge, & Dudley, 1998, p. 556), one has actually been observed. Following a highly active
hurricane season in 1995, green iguanas appeared on Antigua, a Caribbean island, for the first
time. Local fishermen named the exact date of arrival, having seen lizards on a log mat in the
bay (Censky et al., 1998). Green iguanas, it is worth noting, average about 6 kg (13 pounds) in
the wild, comparable to the New World’s woolly monkeys and bald-headed uakaris, and
greatly exceeding the weight of most other New World primate species (Sears, Finarelli, Flynn,
& Wyss, 2008). Furthermore, the possibility of even longer migrations than one between
Caribbean islands is posed by the discovery of North American Douglas firs on Hawaiian
beaches, and a South American log on the beaches of Tasmania (Coyne, 2009, p. 105).
All that was required of the cross-Atlantic trip from Africa was the survival of one or more
mating pairs of a single species, from which all of the New World monkeys descended.
Calculations accounting for prevailing winds and currents indicate that 44 million years ago, a
floating island could have crossed the narrowest gap between Africa and South America in
about nine days (Houle, 1999).
Could a small group of monkeys have survived a journey of that length? Probably so, for
modern mammals of 280 grams (10 ounces), about the size of the New World common
marmoset and thought to be the size of the first platyrrhines (Silvestro et al., 2019; see
Figure 4.7), can survive around 13 days without food and water. Furthermore, vegetation on
Figure 4.7 First related group of New World monkeys: Common marmoset.
Source: Common marmoset (Callithrix jacchus).jpg, CC BY 2.0, Leszek Leszczynski.
the floating island would likely prolong the survival period (Houle, 1999). A transatlantic
journey from Africa to South America is therefore the most likely scenario for the origin of
platyrrhines, the New World monkeys.
A migration from Africa need have happened only once across many millions of years to
introduce primates into South America. There is evidence, however, that it actually
happened twice. The now-extinct Ucayalipithecus, a genus of anthropoids, left fossils in
South America dating to about 32 million years ago. It split from an African lineage
35 million years ago, so that a second rafting must have occurred within that three-
million-year gap (Seiffert et al., 2020). That is about 10 million years later than the original
rafting of the ancestors of the other New World primates, the platyrrhines, implicating a
second migration.
As their name indicates, living platyrrhines have flat noses with widely separated
nostrils. They are generally small and arboreal, and most are diurnal. They typically have
long tails that are often prehensile (able to grasp objects). A wide range of locomotion
occurs across species, including clinging and leaping, quadrupedal branch-walking, and
suspension and brachiation (swinging from branch to branch). Food sources also vary
widely across species, and include leaves, fruit, tree gum, and insects (Rosenberger &
Hartwig, 2002).
The classification of the New World species has been controversial in recent years and has
given rise to competing sets of family names. However, molecular clock approaches make it
clear that the group containing marmosets and tamarins, and the group containing capuchins
and squirrel monkeys, are more closely related to each other than either are to a third group
containing spider monkeys, muriquis, and howler monkeys (Chatterjee, Ho, Barnes, &
Groves, 2009; Pozzi et al., 2014). Several species are illustrated in Figures 4.7 to 4.12.
Figure 4.8 First related group of New World monkeys: Emperor tamarin.
Source: Tamarin portrait 2 edit3.jpg, CC BY-SA 4.0, Brocken Inaglory.
Figure 4.9 Second related group of New World monkeys: Capuchin monkey.
Source: Capuchin Costa Rica.jpg, CC BY-SA 3.0, David M. Jensen (Storkk).
Figure 4.10 Second related group of New World monkeys: Common squirrel monkey.
Source: Saimiri sciureus-1 Luc Viatour.jpg, CC BY-SA 3.0, Luc Viatour/ www.Lucnix.be.
Figure 4.11 Third group of New World monkeys: Ornate spider monkey.
Source: Panama spider monkey, Costa Rica.jpg, CC BY-SA 3.0, Steven G. Johnson.
Early catarrhines
Ancestral Catarrhini meanwhile, were continuing their radiation (expansion in the number of
species) in the Old World regions of Africa, Asia, and Europe. We are fortunate to have substantial
fossils of an early catarrhine, Aegyptopithecus, dating from 29 to 33 million years ago (Simons,
Seiffert, Ryan, & Attia, 2007; Rasmussen, 2002a). A nearly complete male skull was found in
Egypt in 1966 (Figure 4.13). It was from an individual estimated to weigh 3 to 6 kg (7 to 14 pounds),
possessing the heavy limbs of a slowly moving arboreal quadruped. Its upper teeth were ape-like as
were its feet, and it was probably frugivorous (eating fruit; Cowen, 2005; Rasmussen, 2002a).
Early catarrhines existed for millions of years before their descendants split into two groups, one
ancestral to the living Old World monkeys, and one ancestral to the apes including humans.
Aegyptopithecus is a potential candidate for a common ancestor of both groups. In support of this,
the shape of its femur places it almost exactly midway between those of living Old World
monkeys and apes, suggesting that it was the form from which both groups diverged (Almécija
et al., 2019).
Figure 4.12 Third group of New World monkeys: Black howler monkey.
Source: Black Howler Monkey (adult male) 4.jpg, CC BY 2.0, Ryan E. Poplin.
Figure 4.13 Aegyptopithecus skull at the University of Zurich.

Source: Aegyptopithecus face (University of Zurich)-1.JPG, CC BY-SA 3.0, Guérin Nicolas.
Of course, our primary story line continues with the apes. However, the Old World
monkeys are important because they will figure prominently in later cognitive comparisons.
Old World monkeys

Like early catarrhines, today’s Old World monkeys are native to Africa, Asia, and Europe. A
number of species were subjected to genetic analysis by Xing et al. (2005), with results generally
supporting previous cladistic analyses: Old World monkeys exclusive of apes comprise the
family Cercopithecidae, and there are two subfamilies, the Cercopithecinae and the Colobinae.
The Cercopithecinae consist of about 70 species, most living in Africa south of the Sahara
although some live in Asia. One (the Barbary macaque) lives in north Africa as well as the
island of Gibraltar, technically in Europe. Generally speaking, they are diurnal and omni-
vorous but many are primarily frugivorous, and they have cheek pouches for storing food.
They live in highly varied climates and terrains, so that some are arboreal while others are
terrestrial. They have short to medium length tails, and typically have ischial callosities, callused
skin patches on their buttocks that serve as padding while sitting. Figures 4.14 and 4.15
illustrate two well-known species.
Figure 4.14 Rhesus macaque.

Source: Macaca mulatta in Guiyang.jpg, CC BY 2.0, Einar Fredriksen.
Figure 4.15 Guinea baboon.

Source: Male Guinea Baboon in Nuremberg Zoo.jpg, CC BY 2.0, Jakub Friedl.
The Colobinae comprise nearly 60 species living in Africa and Asia. They are primarily
folivores (leaf eaters) and have a specially adapted stomach with multiple chambers to ferment
food. Unlike cercopithecines, who have well-developed thumbs, colobines have small or
vestigial thumbs. Nearly all are arboreal, and while they inhabit diverse climates they do not
live in dry or desert areas as do some cercopithecines. They usually have very long tails.
Figure 4.16 shows one such species.
The ape divergences

Finally we come to the apes, comprising the superfamily of Hominoidea (hominoids). Apes
differ from monkeys in not having tails. They also lack well-developed ischial callosities,
although lesser apes have reduced ones. They also have stiffer backs, with broader and
shallower chests and pelvises (Walker & Shipman, 2005).
Early apes
Apes diverged from monkeys about 29 million years ago, but their first substantial fossils
date to about 20 million years ago. The skeleton of Proconsul (Figure 4.17), from Kenya,
reveals a much larger body than earlier primates, ranging from 9 to 90 kg (20 to
200 pounds) depending on the species and gender (Harrison, 2002). It and related early
Figure 4.16 Grey langur.

Source: MNP Grey Languer.JPG, CC BY-SA 3.0, Marcus334.
Miocene genuses, such as Ekembo (McNulty, Begun, Kelley, Manthi, & Mbua, 2015),
were adapted to living in trees, and were probably slow climbers and above-branch ar-
boreal quadrupeds (Andrews, 2020). Proconsul had curved fingers and an opposable
thumb, and it was tailless (Andrews, 2020; McNulty et al., 2015).
Although Proconsul is a strong candidate for an ancestor of the living apes including
man, its unspecialized skeleton has led some to propose an alternative. Morotopithecus,
from Uganda, was a large-bodied (40 kg, 90 pound) ape also dating to a little over
20 million years ago. Its shoulder was highly mobile, consistent with brachiation or
arm-hanging but contrasting with the quadrupedalism of Proconsul (Gebo et al., 1997;
MacLatchy, 2004). Certainly brachiation or arm-hanging is a plausible character for an
ancestral ape. Phylogenetic analysis, largely based on teeth, does suggest that
Morotopithecus was a closer relative than Proconsul of living apes including humans (Stevens
et al., 2013). However, nothing like a complete skull is available to make the case more
convincing.
It is worth asking why apes arose at all, when Old World monkeys already existed in
similar arboreal environments. Wouldn’t the smaller bodies of monkeys allow them to
outcompete any emerging apes? Kevin Hunt (2016) pointed to a key ape adaptation,
Figure 4.17 Proconsul reconstruction at the University of Zurich.

Source: Proconsul skeleton reconstitution (University of Zurich).jpg, CC BY-SA 3.0, Guérin Nicolas.
namely the ability to assume eccentric grasping postures. That allows them to suspend
from multiple slim supports to forage at the extreme ends of fruit tree branches
(Figure 4.18). When this adaptation began to appear, ape and monkey body sizes were
likely similar, but apes thrived because of it. According to Hunt, the ensuing 20-million
year competition resulted in a splitting of environmental resources. Monkeys began
consuming most of the fruit near the core of trees, and developed the ability to consume
unripe fruit. Apes, on the other hand, consumed ripe fruit at the tree periphery. A
difference in body size evolved, with monkeys remaining small so they could feed
while balanced on branches in sitting postures (e.g., Figure 4.17). Apes became large not
only to physically displace monkeys, but to reach slender branch supports at greater
distances.
Lesser apes
Among living species, the small-bodied gibbons and siamangs (5 to 11 kg, 12 to 25
pounds) are considered “lesser” apes as opposed to the great apes (orangutans, gorillas,
chimpanzees, and humans). Their divergence from the human ancestral line was about 20
million years ago (see Table 4.2). The four genuses are composed of agile brachiators.
Gibbons (Figure 4.19) live in portions of an area roughly defined by northeast India, to
southern China, to the island of Java. Siamangs live in part of the same range, specifically in
Figure 4.18 Orangutan in multibranch suspension.

Source: Orangutans, CC BY 2.0, Johannes Marliem.
Figure 4.19 White-handed gibbons.

Source: Hylobates lar pair of white and black 01.jpg, CC BY-SA 3.0, MatthiasKabel.
Malaysia and Sumatra. These rainforest apes lack cheek pouches for food storage, but males
among the siamangs and some species of gibbons have throat sacs used in making vocal
calls. They are omnivores, typically emphasizing fruit.
Great apes
Our understanding of relationships between the great apes, including humans, has un-
dergone a revolution since the advent of molecular testing. Previously a single branch was
assumed to have diverged from the human ancestral line, representing a common ancestor
of orangutans, gorillas, and chimpanzees. According to that view, none would be more
closely related to us than another. However in the late 1960s, testing of blood proteins
showed chimpanzees to be more closely related to us than are orangutans and gorillas
(Pilbeam, 1972). DNA testing further clarified the relationships, demonstrating a genus-
by-genus divergence from the human line.
The first great ape divergence was of the genus Pongo, the orangutans (or orangutangs),
about 15 million years ago (Table 4.2 and Figure 4.18). There are three similar species,
namely the Bornean and Sumatran orangutans, their names betraying where they live, and
the recently identified Tapanuli orangutan, also a Sumatran species (Nater et al., 2017).
They are the only Asian great apes other than humans. Forest dwellers, they are highly
arboreal (the Tapanuli orangutan perhaps exclusively so), engaging in hanging and branch-
swinging behaviors and often supporting part of their weight (up to 90 kg, or 200 pounds)
with their feet (Figure 4.18). When on the ground, they walk quadrupedally, putting
weight on their fists instead of knuckles as in other great apes. They are generally solitary
but also strongly territorial, and are primarily frugivorous although they do eat other plant
material, insects, and fungi.
The genus Gorilla was the next to branch off the human ancestral line, about 9 million
years ago (Table 4.2). There are two living species, the eastern gorilla and the western gorilla
(Figure 4.20).
Gorillas live exclusively in the “mid-belt” region of Africa, east and west, usually in
forested areas. They are largely terrestrial, walking by putting weight on their knuckles,
although female and young animals do climb trees to sleep. They are chiefly folivorous but
also eat fruit, insects, and seeds. Males can naturally weigh up to 200 kg (440 pounds),
making them the largest living primates.
The last primate genus to diverge from the human ancestral line was Pan, the chim-
panzees, about 7.5 million years ago (Table 4.2). There are two living chimpanzee species
(Figures 4.21 and 4.22), the common chimp Pan troglodytes, and the pygmy chimp Pan
paniscus, also known as the bonobo (pronounced buh-NO-boh). Common chimps weigh
40 to 65 kg (90 to 145 pounds) in the wild, while bonobos are somewhat smaller,
weighing 30 to 45 kg (65 to 100 pounds).
A question that sometimes arises is whether common chimpanzees or bonobos better
model our last common ancestor. Since it was their joint ancestor that broke away from
our line, they are in fact equally related to us, a supposition confirmed by genetic com-
parisons (Prüfer et al., 2012). Thus, they and us are co-equal representatives of our
common ancestor.
The genetic comparisons also indicate that the two species diverged from each other about
two million years ago (Raaum, Sterner, Noviello, Stewart, & Disotell, 2005; Stone et al.,
2010). That split may coincide with a lowering of the Congo River due to dry conditions,
allowing bonobo ancestors to cross to the south of the river while common chimpanzee
ancestors remained to its north. If so, geographic isolation occurred when full river flow
Figure 4.20 Western gorilla.

Source: Western Lowland Gorilla at Bronx Zoo 2 cropped.jpg, CC BY-SA 3.0, Fred Hsu.
resumed, permitting speciation (Takemoto, Kawamoto, & Furuichi, 2015). Nevertheless

limited genetic exchange, less than 1% of the genome, likely occurred between the
two species down to around 100,000 years ago (de Manuel et al., 2016).
Chimpanzees live in central and west Africa, are partly arboreal and partly terrestrial, sleep
in trees, and knuckle walk when on the ground. They are omnivorous, and thus while eating
significant quantities of fruit they also consume insects, fungi, and even small mammals. Both
species live in swampy rainforest, but the common chimp is more widely distributed and also
inhabits woodland areas and savanna (grassland with sparse stands of trees).
The final divergence of apes from the human ancestral line, in the form of chimpanzees,
holds great significance for us. From that point forward, the hominins (bipedal apes) were on
their own.
Conclusion
The dinosaur die-off 66 million years ago produced mammalian diversification, easily
noticeable in the fossil record even though it was not explosive in magnitude. The largest
effect on the ancestors of living mammals was to allow an increase in size, about sevenfold
within a million years. But there were also knock-on effects. In particular, mammalian
diversification produced a diversification of lice, and in turn new species of lice acquired
different species of bacteria.
Figure 4.21 Common chimpanzee.

Source: Schimpanse Zoo Leipzig.jpg, CC BY-SA 3.0, Thomas Lersch.
Most closely related to flying lemurs and tree shrews, primates originated some eight
million years prior to the extinction. Early ones were nocturnal, probably aiding their sur-
vival alongside dinosaurs. Purgatorius, dating to 66 million years ago, had a mobile, grasping
foot. Other primate features emerging early on included opposable thumbs, stereoscopic
vision, and relatively large brains. Carpolestes, from 58 million years ago, had a nail in place of
a claw on its big toe. It probably fed at the slender ends of branches, on a mixed diet
emphasizing fruit.
Initial divergences from the human ancestral line included the Strepsirrhini (e.g., lemurs
and galagos) about 68 million years ago, and tarsiers about 66 million years ago. Today
strepsirrhines live in continental Africa, Madagascar and vicinity, and southeast Asia. They
have a dental comb and a varied diet, and many are nocturnal. Tarsiers live on islands in
southeast Asia, are nocturnal, and eat insects and fruit.
The remainder clade, the anthropoids, had adaptations that included more convergent eyes
and a largely diurnal lifestyle. Two species of the extinct genus Eosimias are known from
about 45 million years ago. They were better adapted to horizontal postures, yet still had a
grasping big toe more similar to tarsiers than to living anthropoids. Others among early
anthropoids gave rise to the Old World and New World monkeys.
The platyrrhini or New World monkeys (e.g., marmosets, capuchins, spider monkeys)
diverged from the human ancestral line about 44 million years ago. As their name implies,
Figure 4.22 Bonobos or pygmy chimpanzees.

Source: Bonobo-04.jpg, CC BY-SA 3.0, Photo by Greg Hume.
they have flat noses. They usually have long tails that are often prehensile, and across species
show a wide range of locomotion and feeding styles. How they got to the Americas is an
enduring problem, with current thinking favoring a crossing from Africa on natural rafts of
vegetation.
The remaining catarrhines or narrow-nosed monkeys resided in the Old World (Africa,
Asia, and Europe). Aegyptopithecus, from 29 to 33 million years ago, weighed 7 to 14 pounds,
had heavy limbs, and probably moved slowly in trees. Around that time Old World monkeys
diverged from the human line, and now comprise the Cercopithecinae (e.g., macaques and
baboons) and the Colobinae (e.g., langurs and proboscis monkeys). Both are very diverse
subgroups, defying simple characterization. However, Cercopithecinae tend to have short to
medium length tails, relatively large thumbs, and ischial callosities, while Colobinae usually
have long tails, small or vestigial thumbs, and lack ischial callosities.
Apes diverged from monkeys about 29 million years ago, but their first substantial fossils,
of Proconsul, Ekembo, Morotopithecus, and related genuses, are several million years younger.
They were mostly large-bodied yet were adapted to living in trees. Lesser apes (gibbons and
siamangs) split off about the same time, 20 million years ago. They live in Asia and are agile
brachiators.
In contrast to an older view that our fellow great apes diverged from our ancestral line as a
group, molecular data are conclusive that multiple divergences occurred. Thus, orangutans
did so about 15 million years ago, gorillas about nine million years ago, and chimpanzees
7.5 million years ago. Orangutans live in Borneo and Sumatra in southeast Asia. They
are almost completely arboreal, and have a varied diet emphasizing fruit. Gorillas live in the
“mid-belt” of Africa, and are largely terrestrial. They also have a varied diet but emphasize
leaves. The chimpanzees (the common chimp and the bonobo) live in central and west
Africa. They are partly arboreal and partly terrestrial, and are omnivorous. They are
also equally related to us.
5 Humans
Through much of the 20th century, the term hominid was reserved for humans and our
immediate ancestors and relations. That made for a very uncertain clade, because the oldest
indisputably hominid fossils dated from three million years ago (Pilbeam, 1972, p. 104), while
the living apes were thought to be descended from a common ancestor that broke from the
human line 14 to 17 million years ago (Pilbeam, 1972, pp. 88, 98). When during that period
did we transition from a more apelike to a more human form?
Recent advances have provided both a more satisfying and a more troubling way of
defining the human clade. Recognition that the ape genera broke off one-by-one from our
ancestral line, with chimpanzee ancestors last doing so 7.5 million years ago, has allowed
tight definition of the clade as consisting of humans, our ancestors, and our nearest rela-
tions back to the chimpanzee split. With a date that recent – and as we shall see, with fossils
nearly that old – it seems likely that human characteristics emerged relatively soon
thereafter.
However, using the definition “since the chimpanzee split”, while reducing uncertainty, is
also troubling. The complete genomes of humans and chimpanzees have been decoded, and
it is clear that we are genetically very similar. Thus, we share over 99% of our coding
for amino acid sequences contained within proteins (Suntsova & Buzdin, 2020; Wildman,
Uddin, Liu, Grossman, & Goodman, 2003). Responding to this similarity, some proposed
that we rename the two chimpanzee species as Homo troglodytes and Homo paniscus, in effect
admitting them to humanity (Wildman et al., 2003).
In contrast, others downplayed any special similarity between humans and chimpanzees
and instead advocated creating a new hierarchy of taxa taking into account the separate
divergences of the Asian and African apes. Under this scheme the family Hominidae would
refer to all great apes including humans (and orangutans), the subfamily Homininae to
all African apes including humans (excluding orangutans), and the tribe Hominini to all
bipedal apes.
Whatever its merits, that proposal has now been widely accepted and the terminology
settled. Accordingly, for our purposes the term hominin (derived from Hominini) refers to
humans and their bipedal ancestors and relatives back to the chimpanzee-human split.
Nevertheless it should be kept in mind that historically, the term hominid was commonly
used, even recently, to refer to the identical classification.
In this chapter we will consider the characteristics of hominins from the Miocene through
the Pliocene, Pleistocene, and today, with special attention to key species. Recent discoveries
of late-living, small-brained hominins will be described. Trends over time will be identified,
including a generalized, disproportionate increase in brain size relative to body size. Finally,
possible ancestral connections will be explored.
DOI: 10.4324/9781003137863-6
The first (Miocene) hominins
Within the past quarter century four spectacular finds have taken the human lineage back
almost to the chimpanzee-human divergence, placing it firmly within the Miocene geolo-
gical epoch. The earliest species, named Sahelanthropus tchadensis, is remarkable for the pre-
servation of a crushed but nearly complete skull nicknamed “Toumai” (Figure 5.1). The
nickname means “Hope of life” in the Goran language used in the area of Chad, north
central Africa, where the fossil was found.
Whether Sahelanthropus should be considered an early hominin or a nonhominin ape has
been controversial (Wolpoff, Hawks, Senut, Pickford, & Ahern, 2006). That is not surprising
considering the 7-million-year age of the specimen. Close to the chimpanzee-human divide,
species on either side would be nearly identical. Arguments for hominin status include the
presence of a relatively vertical, short face, a prominent brow ridge similar to that found in
most later hominins, reduced canine teeth, thickened tooth enamel, and a downward-
opening, oval-shaped foramen magnum, the opening on the bottom of the skull allowing entry
of the spinal column (Zollikofer et al., 2005). The tooth roots likewise suggest that Toumai
was a hominin, for they share some characters with later hominins that are imperfectly shared
with African apes, and not shared at all with orangutans or with Proconsul (Emonet, Andossa,
Mackaye, & Brunet, 2014).
That constellation of traits has produced general though incomplete consensus that
Sahelanthropus was a hominin. The downward opening foramen seems particularly sig-
nificant, as a possible indication of bipedalism. In quadrupedal apes, and even in brachiating
and clambering apes like orangutans, it opens angled a bit toward the rear, allowing the head
to more easily tilt upward relative to the spine. The foramen is also better centered on the
underneath surface of the cranium than it is in apes, another indication of bipedalism. Indeed,
its location falls well within the range of modern humans (Neaux et al., 2017).
Figure 5.1 Skull of Sahelanthropus tchadensis, or “Toumai”.

Source: Sahelenthropus tchadensis-MGL 95214-Download P4150633-white.jpg, CC BY-SA 3.0 FR, Rama.
Humans 67
Toumai’s thickened tooth enamel also seems consistent with bipedalism, because it implies
reduced fruit consumption and thus less time spent in trees. If Sahelanthropus was bipedal, the
freeing of the hands from contact with the ground was a watershed event that allowed new
possibilities for carrying and eventually manufacturing objects – which in turn would have
profound cognitive implications. However, its brain was small, only 365 cc (about ¾ of a
pint) and thus about the size of a bonobo’s.
An alternative approach to classification is to mathematically model species divergences
using as many quantified characters as possible. Strait and Grine (2004) modeled divergences
using 198 characteristics of the cranium (bony braincase) and teeth of a number of living ape
species, fossil hominins, and living humans. The resulting cladogram (Figure 5.2) was largely
replicated in later studies using additional characteristics (Dembo, Matzke, Mooers, &
Collard, 2015; Mongle, Strait, & Grine 2019). It shows the apes diverging from the human
line in the expected order – gibbons, orangutans, gorillas, then chimpanzees – followed
immediately by Sahelanthropus tchadensis. Because the splitting off of Sahelanthropus postdates
the splitting off of chimpanzees, this result lends support to the interpretation that Toumai
was a hominin.
Ardipithecus
The second major Miocene find was of Ardipithecus, shown by the cladogram as branching
off the human ancestral line soon after Sahelanthropus. The oldest examples date to about
6.3 million years ago and are from Ethiopia. Initially only one species was described,
Ardipithecus ramidus (White, 2002). Subsequently a case was made that the earliest examples
should be designated a separate species called Ardipithecus kadabba, with ramidus reserved for
later ones (Haile-Selassie, Suwa, & White, 2004). Others however consider these subspecies,
not separate species (Harcourt-Smith & Aiello, 2004).
The Miocene fossils of Ardipithecus consist of a jawbone, teeth, parts of an upper limb, and
a foot bone. Later ones, about 4.3 million years old, include a partial skeleton including a
pelvis, femurs, and portions of a cranium. Many believe bipedalism is indicated (Lovejoy,
Suwa, Spurlock, Asfaw, & White, 2009), but others are skeptical (Gibbons, 2009). Analysis of
the pelvis suggests that if it was bipedal, it likely walked with a bent-hip, bent-knee posture;
i.e., without a modern stride (Lewton & Scott, 2017).
Figure 5.2 Cladogram of living apes, fossil hominins, and humans, based on cranial and dental characteristics.
Source: Licensed from Elsevier under STM Permissions Guidelines.
Figure 5.3 The foot of Ardipithecus, showing its splayed big toe.
Source: Ardipithecus Fuß.jpg, CC BY-SA 3.0, Tobias Fluegel.
A key point of contention is that a 4.4-million-year-old specimen had a long, splayed,

grasping big toe (Figure 5.3; Lovejoy, Latimer, Suwa, Asfaw, & White, 2009). That may be
more consistent with a tree-dweller than a habitual biped (Hawks, 2009), a conclusion re-
inforced by its curved fingers and other hand characteristics that suggest a vertical climbing
and suspensory lifestyle (Prang, Ramirez, Grabowski, & Williams, 2021). As we shall see,
both earlier and later hominins left footprints showing very little splay of the big toe, sug-
gesting that Ardipithecus may have been a side branch of hominin evolution not on our direct
ancestral line (Begun, 2010).
Orrorin
The third spectacular find from the Miocene was of a species named Orrorin tugenensis. It is
missing from the analysis of Strait and Grine because a cranium has not been found. Instead
Humans 69
Figure 5.4 Top portion of a modern human femur, showing the short femoral neck.
Source: Adaptation of Fumur Posterior annoted.png, CC BY SA-3.0, Frank Gaillard.
its fossils consist primarily of limb bones and teeth from several individuals. Discovered near
Tugen, Kenya, in a tuff (a layer of rock formed from compacted volcanic ash), they are dated
at between 5.7 and 6.0 million years.
Senut (2006) summarized several bipedal features of Orrorin’s femur, the thigh bone
that forms a ball joint with the pelvis. One such feature concerns the femoral neck, the
short span of bone between the shaft and the femoral head (Figure 5.4). Orrorin’s
neck is noticeably longer than that of chimpanzees. Its length is characteristic of early
hominin bipedalism because it allowed the bottom of the femur to angle back toward the
body’s midline, centering body weight in a more columnlike fashion over the legs.
Interestingly, following modification of the pelvis during human evolution, the femoral
neck no longer needs to be so long to achieve the same effect and so it has again
shortened in modern Homo sapiens (Holliday, Hutchinson, Morrow, & Livesay, 2010;
Richmond & Jungers, 2008). This reflects a trend that began in mid-Pleistocene Homo
(Marchi et al., 2017).
Some unknown hominin species – with only chronology leading to the speculation it
might be Orrorin – is thought to have been responsible for the fourth spectacular Miocene
discovery, a possible trackway of footprints recently found near Trachilos, Crete. Dating to
5.7 million years, the impressions show only modest splay of the big toe, much less than that
of Ardipithecus. The find is notable not only for its antiquity but its location, the island of
Crete not having previously been implicated in hominin evolution. Its island status is not
problematic, though, in that it was likely connected to the Greek mainland at the time, and
could have been reached by walking (Gierlinski et al., 2017).
However, Meldrum and Sarmiento (2018) have been critical of Gierlinksi et al.’s inter-
pretation of the Trachilos impressions. Among other factors, they point to ambiguities in
shape that raise questions not only about the prints’ hominin origins, but whether they are
footprints of any kind. For their part, in an exhaustive review of research on hominin feet,
DeSilva, McNutt, Benoit, and Zipfel (2018) seemingly accept the impressions as footprints,
but call for additional information before concluding that they were made by hominins. That
may be forthcoming, in that additional footprints are rumored to have been discovered on
Crete (Chung, 2018).
Taken together, the Miocene hominin discoveries have been nothing short of revolu-
tionary, and they settle an old controversy (Box 5.1).
Box 5.1 The Missing Link
The term missing link was coined in the 19th century, soon after the publication of
Charles Darwin’s Origin of Species ( Lewin & Foley, 2004). It was recognized that if the
nonhuman apes split off from the human ancestral line millions of years ago, there
should surely be fossil evidence of it. The lack of such evidence led to the conclusion
that there was a missing transitional form that sooner or later would be discovered by
scientists working in the field. However, for some members of the public who doubted
evolutionary accounts of human origins, the missing link became a rallying point. As
long as it remained unknown, the gap between apes and humans was something
science had not fully explained.
For scientists, on the other hand, the missing link proved a means of capturing the
public imagination, and a succession of fossil finds were popularly billed as the missing
link ( Reader, 1981). Thus, the discovery of “Java man” (now called Homo erectus) in
1892 provided what then appeared to be the missing link. Yet over the next century,
further discoveries were made, e.g., Australopithecus africanus in 1924, Australopithecus
afarensis in the 1970s, and Ardipithecus ramidus in 1994 ( Lewin & Foley, 2004). Early in
this process, William Jennings Bryan, the famous anti-evolution politician and orator,
is said to have asked, “If the missing link has been found, why are they still looking for
it?” ( BBN International, 2008). In truth, each of these was a missing link that pushed
human origins ever earlier. But the missing link, the earliest possible transitional form
with human characteristics, remained elusive.
For some researchers during the early 1970s, these discoveries seemed to only
nibble at a much deeper problem. The australopithecines, the earliest hominins
known at that time, dated back only three million years. The view then current, that
the ancestor of all nonhuman apes diverged from our ancestral line prior to 14 million
years ago, set off debate over which fossils of that age were closest to representing
the missing link. Pilbeam (1972) argued that the closest was Ramapithecus (now
considered Sivapithecus; Simons, 1992), an orangutan-like creature dating from
14 million years ago. However, the remains were fragmentary, and it was assumed
that future fossil discoveries would more firmly establish the human-ape split as
having occurred around that time.
Today, the reason those fossils have never been found is clear: They do not exist.
Because the ancestor of chimpanzees split from our ancestral line about 7.5 million
years ago, the first fossils with unmistakably human characteristics must be younger
than that split. The Miocene hominins appear to neatly fill the role. The missing link is
no longer missing.
Hominins of the Pliocene

In the Pliocene geological period (2.6 to 5.3 million years ago) first appeared four species in
the cladogram in Figure 5.2, namely the australopithecine species anamensis, afarensis, and
africanus, as well as Kenyapithecus platyops. To these could possibly be added two other aus-
tralopithecines, aethiopicus and garhi. Aethiopicus originated in the Pliocene 2.7 million years
ago, but was mostly of the early Pleistocene. Garhi is technically an early Pleistocene species
due to its dated fossils of 2.5 million year age, but the cladogram implies it diverged from our
ancestral line at an earlier time, between afarensis and africanus.
Humans 71
Note that as Figure 5.2 indicates, certain australopithecine species are sometimes as-
signed to the genuses Praeanthropus and Paranthropus rather than Australopithecus (Harcourt-
Smith & Aiello, 2004; Strait & Grine, 2004; Wood & Boyle, 2016). Also, two other
Pliocene australopithecines, bahrelghazali and deyiremeda, have been proposed, but
are not yet widely accepted as distinct from each other and from afarensis (Wood &
Boyle, 2016).
Cladograms indicate at a glance what forms were (or are) intermediate to others, based on
an integration of many different physical characters. They provide a useful overall sum-
marization, and signpost the order of emergence of lineages. However, it is important to
recognize that cladograms do not themselves identify ancestral forms, any more than
Figure 5.2 argues that chimpanzees descend from gorillas. Thus, the branch points are only
that, branch points leading to species.
The truth is that tracing species-to-species descents through fossils is a very tricky business,
one prone to the emphases and biases of individual scientists. To an outsider it may on
occasion seem to fall to the level of “My fossil is more important than your fossil” or even
simply “I’m right and you’re wrong”. Cladograms can certainly limit the possibilities. For
example, Figure 5.2 would make it difficult to argue that Australopithecus garhi descended
from Kenyanthropus platyops even though the fossils of Kenyanthropus are older. But clado-
grams by themselves can’t prove descent.
Nevertheless it is true that some species-to-species connections are more plausible than
others, generating if not a complete consensus then a preponderance of opinion. Such cases
will be highlighted as we progress through the Pliocene species.
Anamensis
Anamensis is known from a cranium, jaws, teeth, and a partial femur found in Kenya and
Ethiopia, dated to 3.8 to 4.2 million years ago. The recently discovered cranium shows a
sagittal crest (a ridge of bone running front-to-back on the top of the skull), serving as an
additional attachment point for jaw muscles). From associated fossils anamensis is believed to
have lived in a woodland environment. Given its location and characteristics an anamensis to
afarensis descent is considered plausible, although other possibilities exist (Haile-Selassie,
Melillo, Vazzana, Benazzi, & Ryan, 2019; Wood & Boyle, 2016).
Afarensis
Afarensis has the next oldest set of fossils, dating to 3.0 to 3.7 million years ago, with a
3.9 million-year-old skull bone only tentatively identified as coming from the species.
The fossils come from Tanzania, Kenya, and Ethiopia (White, 2002; Wood & Boyle,
2016). The most famous example is the partial skeleton of “Lucy”, including a femur
with an early biped’s distinctively long neck and a shaft that angled in to a horizontal
base (Figure 5.5). The shape of the pelvis is also consistent with bipedalism. Any re-
maining doubt is all but eliminated by Mary Leakey’s discovery of footprints at Laetoli,
Tanzania (Figure 5.6). Imprinted in ash, allowing firm dating at 3.66 million years
ago, the footprints comprise a trackway of two bipedal individuals apparently walking
side-by-side, with a smaller individual stepping in their footprints (Potts, 1992; Masao
et al., 2016). Like the 5.7 million year old Trachilos prints, but in contrast to ramidus
anatomy, the big toe showed relatively little splay. The Laetoli prints are attributed to
afarensis because that species is associated with the geological setting in which the
prints were found, and because its foot was moderately arched like the ones that made
the prints.
Figure 5.5 “Lucy”, Australopithecus afarensis.

Source: Lucy blackbg.jpg, CC BY-SA 3.0, 120.
Afarensis is one of the best known hominins due to extensive fossil remains. It is es-
timated to have stood 1–1.5 m (3–5 feet) in height depending on gender (with males
larger), and to have averaged 35–40 kg (75–90 pounds) in weight. Its brain is estimated
at somewhat over 400 cc (almost a pint) in volume, although cranial remains are in-
complete. It had noticeable brow ridges, and some individuals had a small sagittal crest
(Figures 5.7–5.8). Relatively small, unspecialized teeth suggest an omnivorous diet, and
fossil pollen collected at Hadar, Ethiopia, one of the main sites, indicate it was able to live
in a varied environment that included grassland, temperate woodland, tropical woodland,
Humans 73
Figure 5.6 Replica of a portion of the footprints at Laetoli.

Source: Laetoli footprints replica.jpg, CC BY-SA 3.0, Momotarou2012.
swamp, and evergreen forest among others (Villaseñor, Bobe, & Behrensmeyer, 2020). Its
hand was remarkably modern-looking, with a thumb extending beyond the knuckles
(unlike chimpanzees) but with narrow fingertips (like chimpanzees). Its long arms suggest
it may have been partially arboreal, perhaps sleeping in trees at night like chimpanzees
(Fleagle, 1992; Trinkaus, 1992; Wood, 1992). This supposition is supported by the fossil
remains of a juvenile, showing evidence of bipedalism in the foot and leg, but of arboreal
existence in the shoulder blade and hand (Alemseged et al., 2006). This species, or
possibly Kenyanthropus platyops, is currently believed to be the earliest known hominin
stone tool maker (Lewis & Harmand, 2016).
Figure 5.7 Cast of skull of Australopithecus afarensis.

Source: Australopithecus afarensis reconstruction.JPG, CC BY-SA 3.0, Pbuergler.
Garhi
Garhi, the next australopithecine to split from the hominin line according to the cladogram
(Figure 5.2), is known from a relatively late fossil cranium and palate found in Ethiopia,
about 2.5 million years old. It differs from other species of the period in having large teeth,
especially in the back of the jaw. Its brain size is estimated at 450 cc, about a pint in size
(Asfaw et al., 1999). Garhi may have manufactured stone tools, found in the same area
of Ethiopia and dated to about 2.6 million years ago, but the connection is not certain
(Semaw, 2000).
Africanus
Africanus is the first-discovered australopithecine, described by Raymond Dart in 1925 from
South African fossils. Next to branch off our ancestral line according to the cladogram, it
dates to 2.4 to 3.0 million years ago (White, 2002; Wood & Boyle, 2016). Together, africanus
and afarensis comprise what traditionally have been called the gracile (slender) forms of
Australopithecus, as opposed to the robust (heavily built) forms of robustus and boisei. However,
as we will shortly see, this division is a bit of a misconception.
Africanus stood 1.1-1.5 m (3.5-5 ft) in height, averaged 35-40 kg (75-90 pounds), and
had a brain 420-515 cc in volume. Its face was shorter than that of afarensis. It was certainly
bipedal. In all likelihood it ate fruit and leaves, but carbon isotope analysis suggests that it
also consumed the roots of grass or grasslike plants (or perhaps animals feeding on them).
Humans 75
Figure 5.8 Reconstruction of Australopithecus afarensis.

Source: NHM-Australopithecus afarensis Modell 1 a.jpg, CC BY-SA 4.0, Wolfgang Sauber.
In turn that suggests that africanus lived in a grassland or woodland environment (Wood,
1992; Wood & Aiello, 1998).
Hominins of the early Pleistocene

The early Pleistocene was marked by further australopithecine diversification. Robustus, boisei,
and aethiopicus are often considered to be later-living members of that genus, although many
classify them as genus Paranthropus. The robustus and boisei fossils date to about 1.0 to 2.3 million
years ago, with aethiopicus older at 2.3 to 2.7 million years (Wood & Boyle, 2016). Robustus has
been found in South Africa, and the others primarily in Kenya and Ethiopia.
These species had massive jaws and very large back teeth. Most individuals had a pro-
nounced sagittal crest, indicating that large jaw muscles were used to process a diet heavy in
fibrous plants. The species were of course bipedal, and had brains between 410 and 530 cc
in volume. Traditionally these were considered “robust” forms with heavily built bodies
for their height of 1.1-1.4 m (3.5 to 4.5 ft). However that was somewhat misconceived,
because early weight estimates based on their outsized jaws were inflated compared to later,
more accurate estimates based on skeletal remains. For robustus and aethiopicus the estimates
are 35–40 kg or 75–90 pounds, the same as for the “gracile” forms. Boisei, however, does
appear to have been a bit heavier at about 42 kg or 95 pounds (Harcourt-Smith & Aiello,
2004; McHenry & Coffing, 2000; White, 2002).
In the cladogram, robustus, boisei, and aethiopicus form a separate clade along with
Kenyanthropus platyops (Strait & Grine, 2004), reflecting a general consensus that they re-
present a separate, dead end branch of the hominin tree. Platyops actually dates from the
Pliocene at about 3.4 to 3.5 million years old, and is known only from a highly distorted fossil
skull (Wood & Boyle, 2016).
A recently discovered addition to the genus Australopithecus is sediba, from South Africa.
Two partial skeletons and a partial cranium have been reported, dating to 2.0 million years
ago (Wood & Boyle, 2016). Analyses of dental and cranial characters suggest that sediba most
resembles africanus, and that these two South African species may form their own clade (Irish,
Guatelli-Steinberg, Legge, de Ruiter, & Berger, 2013; Kimbel & Rak, 2017).
The emergence of Homo

For our purposes, the most important event in the early Pleistocene was the emergence of the
genus Homo, commencing with the species Homo habilis (Figure 5.9) and Homo rudolfensis.
These were roughly contemporaneous, with fossils of habilis dated to 1.7 to 2.4 million years
ago (Spoor et al., 2007), and those of rudolfensis to about 2.0 million years ago (Wood &
Boyle, 2016). They differ in size, with habilis the smaller form (Dunsworth & Walker, 2002).
Compared to the australopithecines, such as those in Figures 5.7 and 5.8, the face of Habilis
was flatter and the molars were smaller. Comparatively, rudolfensis had broader rear teeth with
thicker enamel.
There is much controversy surrounding the definition of Homo, but a large brain relative
to body size figures prominently in most definitions. Over the previous five million years
hominin brain size was nearly static. Toumai, the earliest known Miocene hominin, had a
brain about 365 cc in volume, and the australopithecines did not top 530 cc and averaged
closer to 450 cc.
In contrast, the average brain size of habilis was 612 cc (about 1-1/4 pints). Although that
appears larger, caution must be observed because brain and body size are strongly correlated:
Bigger species have bigger brains, in part because a bigger body requires a bigger brain for
sensory and motor purposes. Thus, Martin (1981) found that brain mass in grams (g) was
linearly related to body mass in kilograms (kg) raised to an exponent of 0.76, a relationship
holding across a range of placental mammals weighing as little as 5g (1/6 ounce) and as large
as 50,000 kg (55 tons). Similarly, Shoshani, Kupsky, and Marchant (2006) favored an ex-
ponent of 0.67 for placental mammals. In either case, the relationship between brain and
body mass poses a problem when directly comparing brain sizes.
The encephalization quotient

Fortunately there is a way to compare brain sizes across species independent of body size. An
encephalization quotient (EQ) is calculated, involving an equation taking the brain-body size
relationship into account. We could, e.g., use Martin’s finding and define EQ as brain mass
divided by the 0.76 power of body mass.
However, Williams (2002) noted that both the 0.76 and 0.67 exponents are problematic
when applied to primates. Specifically, each results in (a) a disordered ranking of species, with
apes showing less encephalization than many Old World and New World monkeys, and (b)
substantial sex differences, with females having notably larger EQ values due to their gen-
erally smaller body size. A comparative analysis of published exponent values was undertaken,
using as validation criteria a rough ordering of species in learning ability (humans > apes >
Humans 77
Figure 5.9 Replica skull of Homo habilis.

Source: Homo habilis-KNM ER 1813.jpg, public domain, José -Manuel Benito Á lvarez.
rhesus monkeys > squirrel monkeys) and the reduction of sex differences. Williams found
that an exponent of 0.28, the lowest of the values tested, best satisfied both criteria.
Subsequently others similarly found that an exponent of 0.3 fit better than exponents
exceeding 0.6, based on a more sophisticated measure of cognitive ability integrating
nine behavioral categories (e.g., detour, tool use, and object discrimination; Deaner, Isler,
Burkart, & van Schaik, 2007).
Williams (2002) recommended using the following relationship, which is adopted here:
EQ = brain mass in g/body mass in g0.28
In practice brain size in cubic centimeters (cc) can be substituted for brain mass in grams, as
the brain is about the density of water (i.e., one gram per cc). Of course when calculating
EQ it must be kept in mind that sample sizes are generally small and within-species
variability large. Further imprecision comes from estimating brain size using skulls re-
constructed from crushed or incomplete states, and in estimating body mass from mea-
surements of leg bones or even of correlated structures like the orbit of the eye. The
resulting EQ values must therefore be considered imprecise. Nevertheless, general evo-
lutionary trends are obvious (Table 5.1).
Table 5.1 Eocene primates, Aegyptopithecus, Proconsul, and the common chimpanzee compared to hominin
species, arranged by genus and geological period. EQ = encephalization quotient (see text), kya=
thousands of years ago, mya = millions of years ago
Age Brain size Body mass EQ Notes
Comparison primates
Eocene primates 43 mya 8.3 cc 2.5 kg 1.0 3 species
Aegyptopithecus zeuxis 30 mya 30 cc 6 kg 2.6
Proconsul nyanzae 18 mya 167 cc 15 kg 11.3
Pan troglodytes present 366 cc 45 kg 18.2
Miocene hominins (5.3-23 mya)
Sahelanthropus tchadensis 6.8-7.2 mya 365 cc 45 kg 18.2
Ardipithecus ramidus 4.3-6.3 mya 325 cc 50 kg 15.7 also kadabba
Orrorin tugenensis 5.7-6.0 mya n/a 35 kg n/a
Pliocene hominins (2.6-5.3 mya)
Australopithecus anamensis 3.8-4.2 mya 368 cc 42 kg 18.7
Australopithecus afarensis 3.0-3.7 mya 444 cc 37 kg 23.3
Kenyanthropus platyops 3.4-3.5 mya n/a n/a n/a
Australopithecus africanus 2.4-3.0 mya 455 cc 36 kg 24.1
Early Pleistocene hominins (0.8-2.6 mya)
Australopithecus aethiopicus 2.3-2.7 mya 410 cc 38 kg 21.4
Australopithecus garhi 2.5 mya 450 cc n/a n/a
Homo habilis 1.7-2.4 mya 616 cc 35 kg 32.9
Australopithecus boisei 1.3-2.3 mya 521 cc 42 kg 26.4
Australopithecus sediba 2.0 mya 420 cc 33 kg 22.8
Homo rudolfensis 2.0 mya 789 cc 56 kg 36.9
Australopithecus robustus 1.0-2.0 mya 530 cc 36 kg 28.1
Homo erectus 0.3-2.0 mya 987 cc 63 kg 44.7 mainly Asian
Homo ergaster 1.4-1.7 mya 871 cc 61 kg 39.8 African
Middle and Late Pleistocene hominins (0 kya-0.8 mya)
Homo heidelbergensis 200-700 kya 1158 cc 54 kg 54.8
Homo floresiensis 50-700 kya 426 cc 26 kg 24.7 Indonesian island
Homo naledi 253 kya 545 cc 46 kg 27.0
Homo neanderthalensis 40-130/400 kya 1431 cc 76 kg 61.5
Homo sapiens 0-195 kya 1350 cc 54 kg 63.9
Notes: Ages largely from Wood & Boyle (2016); for Eocene primates from http://eol.org; for floresiensis from van den
Bergh et al. (2016) and Sutikna et al., (2016); for erectus from Herries et al., (2020); for naledi from Dirks et al. (2017). Size
and mass estimates for Eocene primates from Harrington, Silcox, Yapunich, Boyer, & Bloch (2016); for Aegyptopithecus
and Proconsul from Begun and Kordos (2004); for aethiopicus from Kappelman (1996); for sediba, near-adult brain size
estimate from Berger et al. (2010), and adult body size retrieved from http://www.profleeberger.com/AusedibaQandA.
html; for erectus and heidelbergensis from Rightmire (2004). Brain size estimates for afarensis, africanus, habilis, rudolfensis,
floresiensis, and naledi from Hawks et al. (2017), for anamensis from Haile-Selassie et al. (2019), and for neanderthalensis from
Wood and Constantino (2004). Body mass estimate for Pan from Williams (2002); for tchadensis from Brunet et al. (2004);
for ramidus from Suwa, Asfaw, Kono, Kubo, Lovejoy, and White (2009), and White et al. (2009); for floresiensis from Falk
et al. (2006); for naledi from Berger, et al. (2015); for neanderthalensis from Cameron & Groves (2004). Most other values
from McHenry & Coffing (2000).
When EQs are calculated in this way, it is clear that habilis did have a large brain relative to
the australopithecines. Thus, while australopithecine EQs are in the range of 21.4-28.1, the
value for habilis was 32.7. The species packed a big brain for its size. The single known
specimen of rudolfensis did as well: It had a substantially larger body but also a larger brain,
resulting in an even greater EQ of 35.2.
In any case the general consensus is that Homo commenced with habilis, meaning “able,
handy, mentally skillful”, a notable example of assignment of a species name because of cultural
Humans 79
capabilities (Dunsworth & Walker, 2002). Of course mental skills are synonymous with cog-
nitive capabilities, and are reflected in the abundant stone tools associated with habilis.
Ergaster and erectus

The next Pleistocene members of Homo were two similar species, Homo ergaster (Figure 5.10)
and Homo erectus. Not as old as the oldest habilis, they were much larger but also more
encephalized (Table 5.1). Ergaster mostly comes from African sites in Kenya, and erectus from
Asian ones in China and Indonesia, although some of the earliest erectus are found in Tanzania
and the Republic of Georgia as well (Antón, 2003). It is thought that the non-African
examples of erectus descended from African forms that left the continent about 1.8 million
years ago, soon after the species’ origin, then disappeared from it altogether about 800,000
years ago (Antón, 2003; Scardia, Neves, Tattersall, & Blumrich, 2020). Erectus survived in
Java until about 310,000 years ago (Indriati et al., 2011).
The differences between the species are subtle, with ergaster showing more primitive
features of the cranium, jaw, and teeth. It was the first known hominin without arboreal
adaptations, indicating full-time bipedalism. Some researchers downplay the differences and
Figure 5.10 Skull of Homo ergaster.

Source: Homo ergaster skull replica, World Museum Liverpool.jpg, CC BY-SA 3.0, Reptonix free Creative Commons
licensed photos.
define only one species, Homo erectus (Wood & Constantino, 2004), with ergaster considered a
subspecies (Lordkipanidze et al., 2013). A similar consideration applies to another claimed
early Pleistocene species, Homo georgicus from Dmanisi, Georgia, likewise not clearly dif-
ferentiated from erectus (Rightmire, de León, Lordkipanidze, Margvelashvili, & Zollikofer,
2017; Wood & Boyle, 2016).
For both species, meat likely played a larger dietary role than previously, providing the
energy required by a large brain (about 850-1000 cc, or 2 pints). There is some evidence they
used fire, but at a much later period than their time of origin (Antón, 2003).
Hominins of the middle and late Pleistocene

Dating somewhat later to the middle and late Pleistocene was Homo heidelbergensis (0.2 to
0.7 million years ago). It is also known as archaic Homo sapiens. As that name implies, it had a
skull close to modern form (Figure 5.11). It still had a small brow ridge, but over each eye
rather than continuously across the face as in erectus. Its brain was nearly as large as that of
modern humans (about 1150 cc, nearly 2 ½ pints). Fossils of this species have been found
at multiple sites in Europe, Africa, and Asia. Some other hominin specimens, including Homo
Figure 5.11 Skull of Homo heidelbergensis.

Source: Homo heidelbergensis Atapuerca 5 IMG 5649 BMNH.jpg, CC BY-SA 4.0, Photo: Erlend Bjørtvedt.
Humans 81
rhodensiensis (0.3 to 0.6 million years ago) and Homo helmei (90,000 years ago) may instead be
heidelbergensis (Wood & Boyle, 2016).
Naledi
Homo naledi is a very recently described form, discovered by spelunkers exploring a South
African cave system. Reached by a torturous underground path, the fossil chamber was
nearly inaccessible due to a narrow entrance chute. Its excavation waited on the results of a
worldwide call for petite scientists with the requisite skills, and six women ultimately ac-
complished the job (Berger et al., 2015; Shreve, 2015).
An assessment of the fossils’ relatively primitive characteristics led some to think
that they dated back as far as two million years ago. Researchers were stunned, then,
when a variety of dating techniques showed that they are only 253,000 years old (Dirks
et al., 2017). Even more shockingly, naledi had a very small brain, averaging 545 cc across
three crania, 40% of the modern human average (Hawks et al., 2017). Even after taking
into account naledi’s relatively small body, its EQ of 27.0 was only 42% of ours
(Table 5.1).
One primitive characteristic of naledi was the marked curvature of its fingers, approx-
imating that of early hominins and nonhuman apes. The condition, which is likely genetic
(Wallace, Burgess, & Patel, 2020), is an adaptation for climbing and suspension from branches
and is therefore diagnostic of arboreality (Feuerriegel et al., 2017; Kivell et al., 2015). That is
an extraordinary conclusion given the species’ recent existence. Nevertheless naledi was a
proficient biped, and had a human-like stride on the ground. In that regard another primitive
characteristic was a long femoral neck, typical of early hominins but not of Homo species
contemporaneous to naledi (Marchi et al., 2017).
Sapiens
Modern Homo sapiens (Figure 5.12) is held to have emerged about 195,000 years ago
(Wood & Boyle, 2016), with Africa our point of origin. The earliest undisputed specimens
are known from Ethiopia and Israel. Although an origin as early as 350,000 years ago
has been claimed for fossils collected from a Moroccan site (Hublin et al., 2017), their status
as Homo sapiens has been questioned (Callaway, 2017). They do appear to have some features
that are not modern (i.e., the presence of a brow ridge and an undeveloped chin).
One problem is that the boundary between heidelbergensis and sapiens is arbitrary, as there is a
continual gradation. It has been argued nevertheless that the range of variation is sufficient to
justify a division into two species (Wood & Constantino, 2004). The emergence of modern
sapiens was accompanied by substantial cultural and cognitive developments which will be
outlined in subsequent chapters. The average brain size has been 1350 cc (nearly three pints).
Neanderthalensis
The middle Pleistocene is also known for the closely related Homo neanderthalensis
(Figures 5.13–5.14). The earliest unambiguous Neanderthal fossils date from about
130,000 years, and ambiguous ones from 400,000 years ago. The species survived until
about 40,000 years ago (Meyer et al., 2016; Wood & Boyle, 2016). Remains largely
come from Europe but some are from western and central Asia.
For many years there was a controversy regarding the Neanderthals’ status, with some
designating them a subspecies of modern humans (White, Gowlett, & Grove, 2014).
Species status seemed confirmed by the earliest research that examined mitochondrial
Figure 5.12 Modern human skull.

Source: Homo sapiens skull (Holocene) 3, CC BY 2.0, James St. John.
and chromosomal DNA from Neanderthal remains. It reported little affinity to living
humans (Green et al., 2006; Orlando, Darlu, Toussaint, Bonjean, Otte, & Hanni, 2006).
However, subsequent study of the full Neanderthal genome did find similarities.
Specifically, Europeans and Asians were found to be more similar to Neanderthals than
were Africans, strongly implying that interbreeding occurred in areas of Neanderthal
habitation. While the species designation remains, it may not represent the final word
in classification given that up to 2% of the genome of non-Africans derives from
Neanderthals (see Box 5.2).
In that regard a distinction should be made between coalescence time, the latest date at
which Neanderthals and humans had completely common ancestry (and thus the date
at which there was no distinction at all between the species), and split time, the latest date at
which there was any genetic interchange between the species. Coalescence time averages
about 580,000 years across five studies using DNA from the Y chromosome (Mendez,
Poznik, Castellano, & Bustamante, 2016), the autosomes (chromosomes other than X and Y;
Green et al., 2010; Noonan et al., 2006), the whole genome (Prüfer et al., 2014), and
mitochondria (Green et al., 2008).
It is unsurprising that coalescence time predates the earliest Neanderthal fossils (130,000-
400,000 years old, depending on their ambiguity). First, as previously indicated, fossils
postdate the first appearance of a species for probabilistic reasons: The initial population is so
Humans 83
Figure 5.13 Skull of Homo neanderthalensis.

Source: Homo neanderthalensis fossil hominid (Pleistocene; Europe) 3, CC BY 2.0, James St. John.
Figure 5.14 Reconstruction of a Homo neanderthalensis woman.

Source: Reconstruction of Neanderthal woman.jpg, CC BY 2.5, Bacon Cph.
Box 5.2 Neanderthals, Denisovans, and Superarchaics: Species

or subspecies?
Ever since the initial discovery of Neanderthals in 1856, there has been controversy
over how the group should be placed in the human family tree. Hermann
Schaafhausen, the German anatomist who analyzed the first Neanderthal remains,
concluded that in spite of the presence of a heavy brow ridge, they were human – a
race, perhaps, within Homo sapiens ( Goodrum, 2013). However, William King, after
his own examination of the fossils, concluded that they represented a new species,
Homo neanderthalensis. A few years later he went further, stating “I now feel strongly
inclined to believe that it is not only specifically but generically distinct from Man”;
i.e., falling not just outside sapiens but even outside Homo ( King, 1864).
The placement debate continues to the present day. As an undergraduate in the
1970s, I saw the group referred to as both Homo neanderthalensis, a species, and Homo
sapiens neanderthalensis, a subspecies. In 2014, the issue was still alive when Suzanna
White and colleagues reviewed what was meant by “species” and concluded that
Neanderthals fulfilled the major requirements ( White, Gowlett, & Grove, 2014).
Among others, those included the maintenance of distinct anatomical and genetic
differences even after interbreeding.
Yet the issue is still not dead. If anything it is increasingly coming to the fore in
debates over phylogenetic status. Largely this is because of increasing evidence
that sapiens interbred with not just one but multiple archaic groups. Thus, about
2% of the genome of non-Africans and about 0.3% of that of Africans derives
from Neanderthals ( Price, 2020; Skov et al., 2020). But among Oceanics (e.g.,
Melanesians, aboriginal Australians, and Papuans) another 2-4% comes from
Denisovans ( Vernot et al., 2016). The Denisovan group, whose ancestors split
off the Neanderthal line about 420,000 years ago ( Prüfer et al., 2014), and which
survived as late as 29,000 years ago, was first identified by a finger bone and
teeth recovered from a Siberian cave ( Slatkin & Racimo, 2016; Wood & Boyle,
2016). Many stone and bone tools were found as well. Recently, Denisovan genetic
influence has even been found in modern Icelanders ( Skov et al., 2020). Its
contributions to the genome of Homo sapiens, and that of Neanderthals, are illustrated
in Figure 5.15.
Nor does it end there. By accounting for genetic material provided by ancient
groups of sapiens, Neanderthals, and Denisovans, it has proved possible to infer
the existence of another, older interbreeding group whose identity is unknown. This
group, called “superarchaics”, may have directly descended from the hominins
who first migrated from Africa into Europe – possibly early Homo ergaster or erectus
1.9 million years ago ( Rogers, Harris, & Achenbach, 2020) or an even earlier, more
habilis-like species as much as 2.5 million years ago ( Scardia et al., 2020).
For awhile the possibility was entertained that Homo antecessor, the proposed species
name of a one-million-year-old hominid found in Spain, might have been the last
common ancestor of all three groups ( de Castro, Martinón-Torres, Arsuaga, &
Carbonell, 2017; Wood & Constantino, 2004). On that basis it might have proved
to be the superarchaic species. However, analysis of proteins from an antecessor tooth
indicates that the hominin was related to, but not the same as, the last common
ancestor of the three groups ( Welker et al., 2020). For now, the superarchaic species is
unidentified, and the status of antecessor is ambiguous.
Humans 85
Figure 5.15 Denisovan and Neanderthal contributions to the ancestry of Homo sapiens. The numbers
at the left indicate millions of years.
Source: Homo-Stammbaum, Version Stringer.jpg, CC BY-SA 3.0 DE, Chris Stringer.
Given extensive evidence of interbreeding, one criterion for species status – that
groups are genetically isolated so that interbreeding is either impossible or produces
offspring that are not themselves reproductively viable – could lead to the conclusion that
the more recent groups, including Neanderthals and Denisovans, were not separate
species but rather subspecies of sapiens. However some, such as White et al. (2014), have
not considered genetic isolation to be a necessary criterion of species status.
Small wonder, then, that the phylogenetic status of Neanderthals - and indeed, of all of
these groups – is in flux. With respect to Neanderthals specifically, some accept species
status (e.g., Nielsen, Langley, Shipton, & Kapitány, 2020; Terhune, Ritzman, &
Robinson, 2018), others subspecies status (e.g., Abdelhady, Elewa, & El-Dawy, 2019;
Cserhati et al., 2018), and some avoid the matter entirely (e.g., Rogers et al., 2020). This
old debate will likely continue for awhile before scientific consensus is reached.
tiny that finding the first fossils is practically an impossibility. Second, as noted in the dis-
cussion of Toumai, following their split two species are so similar that it may not be possible
to distinguish between them. Thus, older fossils are not only difficult to find, but even if
found might not appear unambiguously Neanderthal.
For its part split time was initially estimated at 370,000 years ago, based on an incomplete
Neanderthal genome (Noonan et al., 2006). However, that conclusion has yielded to re-
cognition that late interbreeding must have occurred between sapiens and neanderthalensis,
possibly as recently as 50,000 years ago (Simonti et al., 2016; Wall & Brandt, 2016).
Neanderthals typically lived in cold, “marginal” environments. They had a larger brain
than sapiens in absolute terms, but a slightly smaller EQ because of their substantially larger
body mass (Table 5.1). They were powerfully built, and their skulls had thick, continuous
brow ridges (Figure 5.13). They left cultural remains including evidence of intentional burials
(Cowen, 2005; Wood & Constantino, 2004).
Floresiensis
The final hominin is also arguably the most bizarre, and not just because it was a late
survival in a world populated by sapiens. A skeleton including a skull of Homo floresiensis
was discovered in 2004 in a cave on the island of Flores, Indonesia, by a team of Australian
and Indonesian researchers. The relatively recent remains were in a prefossilized, extremely
fragile state. Remarkably, even though the specimen was an adult it stood only slightly
over one meter (3 ft) tall and would have weighed only about 22 kg (50 pounds). The
nickname “The Hobbit” was accordingly bestowed because of its diminutive size. The
skull was correspondingly small and had a low cranium (Figures 5.16–5.17), producing an
estimated brain size of only 426 cc, a little less than a pint (Brown et al., 2004; Falk et al.,
2006). The resulting EQ is only 24.7, the smallest of all Middle and Late Pleistocene
species (Table 5.1).
The find was initially greeted by skepticism and a counterproposal that the single in-
dividual might have been a microcephalic (abnormally small-brained) dwarf but nevertheless a
sapiens. Its diminutive stature was subsequently confirmed, however, following the discovery
of partial remains of eight other individuals. Height could be estimated for one of them,
which turned out to be slightly less than that of the original find (Morwood et al., 2005).
Furthermore, measurements based on the skull were found to much more closely match
normal humans than a sample of microcephalics (Falk, et al., 2007). Other analyses based on
the wrist (Tocheri et al., 2007) and the shoulder, foot, pelvis, and femur (Aiello, 2010)
likewise indicate that the Hobbit was not a pathological sapiens.
Initial dating estimates based on charcoal found in the cave found the youngest of the
Flores fossils to be only 12,000 years old. However, this date was discovered to be false,
the result of inadvertent sampling from a different geological section than the fossils. An array
Figure 5.16 Skull of Homo floresiensis.

Source: Homo floresiensis.jpg, CC BY 2.0, Ryan Somma.
Humans 87
Figure 5.17 Artist’s reconstruction of floresiensis.

Source: Homo floresiensis, CC BY 2.0, Ryan Somma via Flickr.
of dating methods now firmly date the youngest of the floresiensis-related deposits at
50,000 years old (Sutikna et al., 2016).
More recently, teeth and a jaw bone of floresiensis excavated in 2014 were described and
dated to the much older period of 700,000 years ago. They were just as small as the later
remains, and if anything a bit smaller. Although they do not address the size or state of the
cranium at that period, they do establish the antiquity of the species on the island of Flores
(van den Bergh et al., 2016).
In 2019, 67-thousand-year-old hominin fossils from Luzon, Philippines, were described as
a new species, Homo luzonensis (Détroit et al., 2019). Aspects of its teeth, and of its foot and
hand bones, variously resembled australopithecines, Homo erectus, Homo sapiens, Homo nean-
derthalensis – and Homo floresiensis. Although believed to have been small-bodied, there are
insufficient skeletal remains to allow either a weight estimate or a close comparison with
floresiensis. It therefore seems inadvisable at this early stage to attribute new species status to
the remains (Gerbis, 2019). The same might be said of the even more recently described
“Homo longi”, of 150,000 years ago, that pairs massive, continuous brow ridges with a very
Neanderthal- and sapiens-like brain size of 1420 cc (Ji, Wu, Ji, Li, & Ni, 2021).
Hominin trends and connections

It is useful to highlight trends over the 7.5 million years of hominin evolution, because as
we will see, they correspond in some degree to the evolution of cognitive capabilities.
They also make it possible to identify the most likely possibilities for ancestral connections
among species.
Size trends
An examination of Table 5.1 highlights a strong trend in brain size. Across species and with
few exceptions, brain size has increased, from a sub-400 cc level in the Miocene to the mid-
400s in the Pliocene, as high as 987 cc in the early Pleistocene, and finally to around 1400 cc
in the later Pleistocene species of Homo neanderthalensis and sapiens. All told this was an
increase from ¾ of a pint to three pints. The trend is so powerful that historically it rightly
assumed a major role in the reconstruction of hominin phylogeny (evolutionary relationships).
Body size has varied as a secondary trend, though in a more complex fashion. Most species
through the early Pleistocene weighed less than 50 kg on average, and several less than 40 kg.
However beginning with the first Homo species after habilis, most exceeded 50 kg with
some over 60 kg. Indeed, it can be argued that some of the gain in absolute brain size was
accomplished simply by upscaling body size.
Considering the size trends jointly, however, indicates that growth of the brain out-
stripped growth of the body. Thus, the ape and Miocene hominin EQ values of a little
under 20 increased to 23-24 in the Pliocene, to over 30 in some early Pleistocene species,
and then with some exceptions to 50 and even upwards of 60 in the middle and late
Pleistocene. The trends reveal something else as well: A portion of the later increase in
encephalization came about not just because absolute brain size increased, but because
body size decreased. The early Homo species of ergaster and erectus had large brains but also
large body masses, resulting in EQs only modestly advanced over that of the first Homo
species, the small-bodied habilis. Mean body mass then decreased by 10 kg in hei-
delbergensis and sapiens, which with a 200-400 cc increase in brain volume boosted their
EQ values to high levels. Interestingly, the intelligence of certain birds such as parrots
seems to have been achieved in a similar way, by shrinking body size but not brain size
(Ksepka et al., 2020).
Notable exceptions to the hominin trends are the late-surviving species Homo naledi
and Homo floresiensis, whose small brains and bodies result in EQs comparable to the aus-
tralopithecines. In fact their EQs are so similar that they raise the question of a possible
affinity between the species. However, phylogenetic analyses produce ambiguous results,
with naledi showing affinities to Homo generally and not to floresiensis specifically (Dembo
et al., 2016; Schroeder et al., 2017).
Naledi was too recently discovered to permit any firm speculation as to its origins. With
respect to floresiensis, however, Falk et al. (2005) suggested that it might represent an example
of island dwarfism. That is an evolutionary phenomenon in which isolation on an island causes
large species to become reduced in size over time. Island dwarfism is specifically observed
among primates (Montgomery, 2013). It probably occurs because islands prevent migration
during famine, resulting in a selection pressure toward lower energy consumption and thus
smaller body sizes.
After performing a cladistic analysis of 60 characters of the cranium, mandible, and
postcranium, Argue, Morwood, Sutikna, Jatmiko, and Saptomo (2009) concluded that the
Hobbit may have split off the line leading to us much earlier than its age implies. They
suggested that Hobbit ancestors may have diverged from the Homo line around the time of
Homo habilis, placing the split at about two million years ago. On this basis the researchers
suggested that the species may have started out and stayed small. A later analysis using an
expanded set of 133 characters came to a similar conclusion (Argue, Groves, Lee, &
Jungers, 2017).
That position receives general support from the aforementioned phylogenetic analysis of
Dembo et al. (2016), finding that the Hobbit is most similar to the over-2-million-year-old
Australopithecus africanus, and next most similar to Homo habilis.
Humans 89
However a number of others report that floresiensis shows an affinity with African Homo
erectus in several respects including the skull and shoulder (e.g., Baab & McNulty, 2009;
Lyras, Dermitzakis, Van der Geer, Van der Geer, & De Vos, 2009), and the teeth and
mandible (van den Bergh et al., 2016). Zeitoun, Barriel, and Widianto (2016) even suggested
that floresiensis should more properly be classified as erectus! According to this interpretation,
what we currently label as floresiensis started as full-size erectus, but became dwarfed due to
island environment of Flores.
Skull trends
Additional trends over the course of hominin evolution are apparent from skulls. The brow
ridges of tchadensis seven million years ago (Figure 5.1) waned, waxed, and waned again
in size over successive species but were consistently present until the emergence of
modern sapiens. At the same time, the face became flatter and more vertical, and the rear
teeth generally decreased in size as diets included more meat and less fibrous vegetable matter.
All of these characters, like brain size, have figured prominently in the reconstruction of
our phylogeny.
Hominin phylogeny
What then was the structure of the human family tree? Before addressing this question it is
helpful to consider some influences on phylogenetic inferences. One already referred to is the
occasional tendency of the discoverers of a fossil to overweight its importance. That can
easily affect how that particular team reconstructs phylogeny. However, the beauty of science
is that others are free to reconsider the evidence to potentially come to more balanced
conclusions.
A second influence is that the age of a species is rarely precisely known even if it left
accurately dated fossils. Earlier and later fossils may never have formed, or may still be in the
ground waiting to be discovered. Thus, the species may have had a longer evolutionary
lifespan than is apparent from fossil evidence.
Third, the assignment of fossils to particular species is error-prone. There are many his-
torical examples of the reassignment of a misassigned fossil following the acquisition of ad-
ditional information. That obviously affects the reconstruction of phylogeny.
Finally, a fourth influence on phylogenetic inferences should be inserted as a cautionary
note. This is that it is generally impossible to determine whether any fossil is from a direct
human ancestor in a strict genetic sense. The best we can say is that any given fossilized
individual, and every human alive today, traces back to a common ancestor at some un-
known point during or prior to the existence of the fossilized individual. This raises questions
as to whether we can say that we descend from a particular species as defined by known
fossils. However, in many cases we can infer that we must descend from an individual very
much like that species. With that proviso it is nevertheless common practice, as a kind of
shortcut, to refer to specific species defined by known fossils when reconstructing phylogeny.
We can now consider the likelihoods, tracing backwards. Homo sapiens (0-195,000
years ago) is almost universally recognized as a descendant of Homo heidelbergensis (0.2 to
0.7 million years ago. In turn, heidelbergensis is assumed to have descended from Homo
erectus (0.3 to 2.0 million years ago), most likely the early African forms since later Asian
ones are probably too derived to be ancestors of modern humans (Wood & Constantino,
2004). Erectus likely descended from the more primitive ergaster, even though at present
its oldest fossils, dated at 2.0 million years ago, predate the oldest ergaster fossils, at
1.7 million years ago.
What path is traced backward from ergaster depends on which characters are emphasized. A
strict chronology-and-encephalization approach traces the line back through Homo habilis.
However, others emphasize the postcranial skeleton (the skeleton below the head) and suggest
that habilis had limb proportions that were too ape-like to make it a likely human ancestor
(Richmond, Aiello, & Wood, 2002). Nevertheless increasing encephalization was clearly a
major hominin theme, and that plus the cultural remains associated with habilis do seem to
justify its placement in the ancestral tree.
There is also controversy with respect to the link between habilis and earlier forms. There
is near-consensus that Australopithecus afarensis (3.0 to 3.7 million years ago) was ancestral,
but less agreement that the 600,000 year gap between habilis and afarensis was filled by
Australopithecus africanus (2.4 to 3.0 million years ago). Some nominate Australopithecus garhi
(2.5 million years ago) for the intermediate role, but remains seem too fragmentary at this
point to draw that conclusion with any certainty.
As earlier indicated, a descent of afarensis from anamensis (3.8 to 4.2 million years ago) is
considered plausible, and in fact the across-three-species ancestral connections between
habilis, afarensis, and anamensis have been accepted by Donald Johanson, one of the dis-
coverers of “Lucy”, based on derived characters that seemingly passed from one to the next
( Johanson, 2017).
Although a connection from anamensis to ramidus (4.3 to 6.3 million years ago) has been
proposed, ramidus’ widely splayed big toe is problematic. For that reason it seems wiser to
place a speculative link from anamensis to tugenensis. What relationship tugenensis – or for that
matter, ramidus – had to Sahelanthropus tchadensis remains to be seen. Wood and Boyle (2016)
raised the possibility that all three should be assigned to the same genus, or even collapsed
into one or two species instead of three, in recognition of their general similarity. But for
now tchadensis (7 mya) can be tentatively placed at the head of the hominin ancestral line of
descent, as the earliest of the three forms.
A well-pruned bush
What is most notable about Table 5.1 is that while many hominin species have existed across
7.5 million years, only one survives. Our portion of the tree of life more resembles a heavily
pruned bush that it does a tree, with a single branch emerging from the crown and all others
trimmed away.
Heavy pruning is not unusual in evolutionary history, another example being the survival
of birds as the only representatives of a once-numerous superorder of dinosaurs. By its
nature evolution often takes a crooked path from past to present. The randomness of mu-
tation combined with diverse and changing environments results in many unsuccessful
“experiments”, a useful term as long as we recognize that no intentionality is involved.
One educated guess is that of all the species ever generated by evolution, 99.9% are now
extinct (Raup, 1991, pp. 3-4).
Of course one difference between birds and humans is that birds radiated to become
thousands of species worldwide, while there is now only one human species. Not only
can any population of humans interbreed with all others, but genetic analyses show close
relatedness in evolutionary terms. For example, studies have examined the similarity of
populations with respect to mitochondrial DNA, the genetic instructions accompanying
the mitochondria in our cells that are not part of our 46 chromosomes. Because mi-
tochondria are inherited as part of the egg cell rather than the sperm, their genetic
content follows the maternal line of descent, mother to daughter to child. (Although boys
don’t have egg cells, they nevertheless derive their mitochondria from their mother’s
egg cell.) Taking a molecular clock approach suggests that living human populations trace
Humans 91
to a common female ancestor, a “mitochondrial Eve”. She is estimated to have lived
sometime between 125,000 and 200,000 years ago. Furthermore, Africans show the
greatest variability in mitochondrial DNA and therefore the deepest convergence on that
ancestor, strongly arguing that she lived in Africa (Cyran & Kimmel, 2010; Ingman,
Kaessmann, Pääbo, & Gyllensten, 2000). In fact, comparison with living populations
suggest she may more specifically have lived in present-day Botswana, in southern Africa
(Chan et al., 2019).
A second line of research has examined population similarities in the sequencing of the
Y chromosome, which is inherited in the paternal line, father to son to son. (Girls do not
have Y chromosomes.) Application of molecular clock principles indicates that a common
ancestor of all men lived 70,000 to 200,000 years ago, but possibly as much as 340,000 years
ago. Furthermore, like Eve this “Adam” is believed to have lived in Africa, possibly in what is
now western Cameroon in the continent’s northwest quarter (Mendez et al, 2013; Poznik
et al., 2013; Scozzari et al., 2014). Furthermore, remains of Neanderthals less than 55,000
years old were recently discovered to have carried an “Adam-like” Y chromosome! The
implication is that the interbreeding that resulted in our Neanderthal genes also allowed
Neanderthals to inherit our apparently advantageous Y chromosome (Petr et al., 2020).
It should be stressed that African origins apply to all of our genetic material, not just
mitochondrial and Y chromosomal DNA. The DNA from our autosomes similarly shows
greatest variability in African populations, implying that it originated there and thus has had
maximal time to develop diversity. Yet even the least diverse population globally – the Suruí,
a Brazilian tribe – captures 60% of total worldwide diversity within its members (Hunley,
Cabana, & Long, 2016), reflecting the relatedness of human populations.
Thus, 7.5 million years of human evolution have come down to just one interrelated
human species. This certainly was not always the case, as hominin ancestry has been bushy in
the past. At least six species were alive two million years ago, and three species as little as
50,000 years ago (Table 5.1).
What accounts for such severe pruning? Undoubtedly part of the answer is that all bipedal
apes have occupied very similar environmental niches. They have been omnivorous, able to
travel distances while carrying babies or tools, and large enough to defend against predators
and doubtless other bipedal apes. Such similarity in the demands placed on the environment,
and in responses to it, created direct competition for resources when different species came
into contact.
Part of the answer, too, must be that the playing field implied by competition became
radically tilted when human cultural innovations became commonplace. In turn cultural
innovations were produced by cognitive innovations, ensuring the selective survival of “wise
man”, or in Latin, Homo sapiens.
Conclusion
The term “hominin” refers to humans, their ancestors, and their immediate relatives, back to
the chimpanzee-human split 7.5 million years ago. The Sahelanthropus tchadensis (“Toumai”)
fossil dates back seven million years, almost to the split itself. Signs of bipedalism in the skull
are echoed in Orrorin fossils a million years later, showing the long femoral neck characteristic
of early bipeds. Ardipithecus is a third Miocene hominin dating to 6.3 million years ago.
However, the species had a splayed, grasping big toe, postdating a recently discovered
trackway in Crete lacking that feature, and thereby suggesting that it may not have been
directly ancestral to modern humans.
Hominin species emerging in the Pliocene included Australopithecus anamensis, afarensis,
and africanus, and Kenyapithecus platyops. Anamensis, dating to 3.8 to 4.2 million years ago,
represents a plausible transition from earlier forms. “Lucy” is the most famous example of
afarensis, consisting of a partial skeleton including a long-necked, bipedal femur. This species
likely made the trackway at Laetoli. Afarensis may also have been partially arboreal, judging
from the shoulder blade and hand, but there is a good chance that either it or Kenyapithecus
made the earliest known stone tools.
Australopithecus garhi (2.5 million years ago) was possibly also an early maker of stone tools.
Its contemporary Africanus was the first-discovered australopithecine, and probably lived in a
grassland or woodland environment in South Africa. The australopithecines robustus, boisei,
and aethiopicus are sometimes assigned a separate genus, Paranthropus, in recognition of dis-
tinctive features including massive jaws and a sagittal crest.
The genus Homo emerged about 2.4 million years ago in the form of Homo habilis, a species
marked by a noticeable increase in encephalization. It was probably the ancestor of Homo
ergaster, itself giving rise after a very brief time to Homo erectus, with the latter surviving in Asia
until relatively recently (about 310,000 years ago). Ergaster was an African hominin that for
the first time showed an absence of arboreal adaptations, indicating full-time bipedalism.
Erectus was a likely ancestor of Homo heidelbergensis, or archaic Homo sapiens, dating as far
back as one million years ago. Modern humans emerged about 195,000 years ago in Africa.
Three other relatively late species were Homo neanderthalensis, naledi, and floresiensis, the
former of which contributed to the biological ancestry of modern sapiens. Naledi and flor-
esiensis were small-brained species with low EQs, and floresiensis also had a very small body,
possibly a case of island dwarfism. A long-standing controversy over the species versus
subspecies status of Neanderthals is receiving new impetus from genetic studies implicating
interbreeding of sapiens with neanderthalensis, with a group called Denisovans, and with yet
another group of “superarchaics”.
Throughout humankind’s descent, brain size has generally increased both in absolute terms
and in relation to body size. EQ values more than tripled between “Toumai” and today, a
trend aided from the onset of archaic sapiens by a reduction in body size. Another trend has
been a consistent trimming of the hominin “bush”, from at least five coexistent species two
million years ago to today’s single species. There is strong evidence that all humans descend
from a common female ancestor, “mitochondrial Eve” living 125,000-200,000 years ago,
and all men from a Y-chromosome “Adam” living 70,000-200,000 years ago.
Determining the hominin line of descent is subject to biases, imprecise dates, and the im-
possibility of determining whether any fossil is a direct ancestor in a genetic sense. The like-
lihood is that modern Homo sapiens descends from Homo heidelbergensis, itself descending from
Homo erectus and then in turn from Homo ergaster and Homo habilis. Habilis was likely descended
from Australopithecus afarensis and Australopithecus anamensis. The remaining connections are
more conjectural, but links to Orrorin tugenensis and finally Sahelanthropus tchadensis are possible.
Section II
Sensation and movement

6 The mechanical and chemical senses
A large brain serves as only a crude indicator of the sensory, motor, and cognitive abilities
Homo sapiens acquired over 7.5 million years of hominin evolution. Our ancestors used
brain specializations, as do we, to collect inputs from the environment, to understand
meaning, and to produce outputs in response. How sensation and movement evolved
provides important context for understanding the evolution of the cognitive faculties that
bridge them. In this chapter we primarily consider the mechanical and chemical senses of
touch, balance, hearing, smell, and taste, and the evolutionary trajectory shared by some
of them.
Early sensing
Even early single-cell organisms needed a way to interact with their environment. Life
depended on it, for metabolism within the cell was contingent on obtaining raw materials
from outside and on eliminating waste products from within. Both these needs required the
ability to sense the presence of substances outside or inside the cell.
The simplest early sense mechanism was mechanical. When pressure inside increased
past tolerable limits, large pores in the cell membrane opened, pouring out some of the
cell’s contents until pressure was lowered. This mechanical gating (the controlled passing of
substances through a membrane) exists in similar form across all three domains of bacteria,
archaea, and eukaryotes, testifying to an ancient evolutionary origin (Balleza, 2011).
At a very early evolutionary point, cell membranes acquired the ability to pass some
molecules but not others. The ability to distinguish between what to pass and what to
block from entering the cell was a crude form of external sensing. Early on, naturally
occurring amino acids and phosphates were candidates for transportation into the cell
(Trevors, 2003).
There is evidence that the cross-membrane transport of ions (electrically charged
atoms), occurred early in the tree of life. Potassium ions (symbolized K+) form when
potassium salts dissolve in water, and are actively transported across cell membranes in all
three biological domains (Hänelt, Tholema, Kröning, Vor der Brüggen, & Wunnicke,
2011). Maintaining appropriate K+ levels within the cell is critical to phosphate transport,
as well as to enzyme-mediated chemical reactions. Derst and Karschin (1998) constructed
a phylogenetic tree of genes involved in K+ transport and tentatively concluded that
some originated in prokaryotes, later descending to eukaryotes about two billion
years ago.
A proton pump – a membrane pump of hydrogen ions (H+) – was probably an additional
early development. Membrane proteins capable of pumping H+ out of a cell are believed to
DOI: 10.4324/9781003137863-8
96 Sensation and movement
have existed in the last common ancestor of all life (Deamer & Weber, 2010; Wei &
Pohorille, 2015). Using an external source of energy such as thermal or light energy from the
sun, H+ was pumped out of the cell. Then when the energy source was no longer available,
such as at night, H+ was let back into the cell, freeing energy to be used in chemical reactions
such as phosphate synthesis.
Other chemical transport mechanisms believed to have had prokaryote precursors are
those for the transport of sodium (Na+) and calcium (Ca+) ions, evolutionary descendants of
the K+ mechanism. By about 600 million years ago, most of today’s ion transport channels
had evolved (Derst & Karschin, 1998).
Even at the unicellular level, the ability to sense compounds outside the cell can have
behavioral consequences. Today’s bacteria are capable of surprisingly sophisticated chemical
signaling techniques to enhance mass action. Quorum sensing refers to the ability to detect
increasing numbers of other bacteria by sensing a building concentration of chemical ex-
cretions. It is used to coordinate the release of toxins when attacking a host, and to establish
biofilms, which are cooperative communities of bacteria, each contributing some component
to the matrix (Bassler & Losick, 2006). It is also used to respond to the deaths of community
members, for example by signaling survivors to move away from antibiotics or to expel them
(Bhattacharyya, Walker, & Harshey, 2020).
An early origin for quorum sensing is suggested by the fact that rhomboid protein, a
signaling chemical, is found across the life domains (Henke & Bassler, 2004). It is even
possible that chemical communication was essential for the emergence of unicellular life.
Communal living would have allowed massed numbers of individual cells, avoiding “ex-
tinction by dilution”, and chemical communication would have provided group protection.
These may be reasons early life is evidenced by the huge colonies of bacteria comprising
stromatolites (Combarnous & Nguyen, 2020; see Figure 1.3).
Touch
Mechanical gating and ion transport probably served as sufficient sense mechanisms for many
early single-cell organisms. However, metazoa, with complex body plans and in many cases
improved mobility, required more complicated sensory systems. These included the presence
of specialized touch receptors, and in most phyla a nervous system to carry touch information
beyond the limits of the cell.
Mechanoreceptors
Mechanoreceptors (specialized sensory receptor cells that react to mechanical forces) predated
nervous systems and possibly contributed to their evolution. The earliest mechanoreceptors
are thought to have been in the form of thread-like cellular outgrowths. These were either
small (cilia) or large (flagella), surrounded by microvilli (tiny projections of cell membrane) that
were used in feeding. The outgrowths had both sensory and motor function, so that their
stimulation caused movement. Their possession by choanoflagellates dates their origin to 1.0
to 1.5 billion years ago (Arendt, Benito-Gutierrez, Brunet, & Marlow, 2015; Fritzsch,
Pauley, & Beisel, 2006).
Hair-based mechanoreceptors may descend from ancestral choanoflagellates, but more
certainly from ancestral metazoans over 600 million years ago. These had a central hair
surrounded by microvilli, and were probably the origin of later touch receptors (Fritzsch
et al., 2006). The ancestors of early cnidarians probably also had hair-based mechanoreceptors
in the form of stinging cells, possibly the origin of neurons (Box 6.1).
The mechanical and chemical senses 97
Box 6.1 The origin of neurons
Miljkovic-Licina, Gauchat, and Galliot (2004) proposed that neurons (nerve cells)
had their origin as mechanoreceptors, specifically in the immediate ancestors of
early cnidarians. Along with some ctenophores (comb jellies), cnidarians were
the first metazoans to have identifiable neural nets. The earlier-emerging sponges
did not.
But how could neurons have evolved from mechanoreceptors? Miljkovic-Licina
and colleagues pointed out that cnidarian stinging cells sense mechanical dis-
turbances. They respond by ejecting barbed tubes or threads that inject venom to
immobilize both attackers and prey ( Figure 6.1). Evolution might have caused
these cells to differentiate, with one line of descending cells evolving into neurons.
In turn these might have connected with the stinging cells, possibly bidirectionally
to allow signals to pass back and forth, improving coordination during attacks
( Liebeskind, Hillis, Zakon, & Hofman, 2016). Partially supporting this supposition,
stinging cells and neurons share the same regulatory genes ( Miljkovic-Licina et al.,
2004).
Figure 6.1 Representation of a cnidarian stinging cell firing sequence (left to right), with hair “trigger”
(cnidocil) and coiled thread ready for ejection.
Source: Nematocyst discharge.png, public domain, Spaully.
However, there is by no means a consensus that neurons evolved from stinging cells.
Some believe they instead evolved in conjunction with muscles, quickly building into
diffuse neural nets controlling movement. Certainly cnidarians and ctenophores both
have nets directly connected to muscle fibers. This arrangement could then have
extended to control the muscles involved in feeding and digestion ( Arendt, Tosches, &
Marlow, 2016).
Whatever view of neuronal origins is correct, continuity between cnidarians and the
bilateria (including chordates and vertebrates) is indicated by the use of the same genes
to specify cnidarian neural nets and bilaterian nervous systems ( Arendt et al., 2016).
Similarities between mechanical sensors found in cnidarians, chordates, and the
vertebrate inner ear likewise suggest a common origin. Thus, the nervous system in
the crude form of a neural net, and its support of mechanical sensing, originated in
shared ancestry a little over 605 million years ago ( Burgihel et al., 2003).
Early-emerging taxa with mechanoreceptors that synapsed onto neurons included

tunicates (or urochordates), including sea squirts, with hair cells arranged in a coronal organ
in the oral region that detected vibration in water and thus motion (Burgihel et al.,
2003). They also included ancestral lancelets, whose descendant amphioxus has similar
cells with microvilli, also located in the oral region (Kaltenbach, Yu, & Holland 2009).
In humans, somatosensation (the sense of touch, or the tactile sense) begins when receptors in
the skin are temporarily deformed due to mechanical pressure (Figure 6.2). Merkel’s cells (or
discs) and Meissner’s corpuscles are two types of touch receptors, both lying just below the outer
skin. They detect fine details and flutter, respectively. Hair follicle receptors are a third type,
consisting of a root hair plexus (nerve endings wrapped around the base of a hair) that respond
to bending. More deeply embedded in the skin are Ruffini’s corpuscles and Pacinian corpuscles,
responding to skin stretching and vibration, respectively. Each receptor is thus a sensory cell
having a specialized function.
Figure 6.2 The skin receptors.

Source: Blausen 0809 Skin TactileReceptors.png, CC BY-SA 3.0, BruceBlaus.
Not much is known about the evolution of touch receptors. However, research has
recently identified a common developmental pathway for Merkel’s cells and inner ear hair
cells, and that may indicate a common evolutionary pathway as well. Specifically, their
development depends on expression of the same specific pair of gene-derived proteins. It
is speculated that the pair originated in ancestral chordates, later giving rise to both types of
cells. It is not known whether early cells had hairs, which Merkel cells lost, or lacked hairs
later added by inner ear hair cells (Yu et al., 2021).
A bit is also known about the evolution of Meissner’s corpuscles. Found in both marsupials
and primates (Hoffman, Montag, & Dominy, 2004), they presumably originated at least
170 million years ago in the common ancestor of both (Drummond et al., 2006). In primates
they are related to frugivory, with more frugivorous species having a higher density of
Meissner’s corpuscles, perhaps to better judge the texture of fruit (Hoffman et al., 2004).
Regardless of type, a skin receptor is stimulated when mechanical pressure impinges on
it either through the skin or by hair movement. That stretches its cell membrane, resulting
in the opening of ion channels that permit sodium ions (Na+) to enter. As a result, a net
positive charge is created inside the cell. With sufficient stimulation the increase in positive
charge, called a generator potential, increases past a threshold value at which point other
Na+ channels open. Even more ions flood into the cell, creating a spike potential (a sudden
increase in positivity), which travels up an axon (a long thread-like projection) on the other
end of the cell.
Evolution produced this Na+ gating mechanism by building on the one present in single-
cell organisms. Thus, a method initially used to detect and admit to the cell ions critical
to metabolism, became an important link in signaling touch.
Tactile neural pathways

In humans, somatosensory cell axons first synapse on neurons in the cutaneous nerves, which
enter the spinal cord. From there they synapse onto neurons of two different systems, called
the medial lemniscal and extralemniscal systems. Axons of the medial lemniscal system run
upward to the medulla of the brain, where there is a synapse onto another set of neurons.
These cross over the body’s midline, travel up through the thalamus, and end in the primary
somatosensory cortex (designated SI), occupying nearly all the postcentral gyrus, the most
forward part of the parietal lobe (Figure 6.3). Because of the crossover, the medial lemniscal
system is contralateral (opposite-sided), with the left side of the body represented in the right
hemisphere of the brain and vice versa.
In contrast, the extralemniscal system is largely unlateralized. Some of the axons in this
system cross over, but others do not, so that each side of the body is represented in each
hemisphere. The final connections of the extralemniscal pathway are to the parietal lobe in an
area designated SII (located in the ceiling of the lateral sulcus adjacent to the postcentral
gyrus, see Figure 6.3), as well as to the rear of the parietal lobe and the frontal lobe.
It is known that SI and SII exist across the mammalian phyla, including marsupials (Kaas,
2004a). Thus, like Meissner’s corpuscles, they have an origin dating back at least 170 million
years. Their size follows a “principle of proper mass” enunciated by Harry Jerison (1973, p. 8).
This states that there is a relationship between the neural mass devoted to a function, and the
amount of processing involved. Accordingly, the most sensitive parts of the human body, such
as the lips and hands, have the greatest cortical representation. In contrast, naked mole-rats,
which live underground in the dark and depend heavily on somatosensation, have greatly
expanded cortical areas representing touch to their incisors and head. Overall, SI is 50% larger
in naked mole-rats than in laboratory rats. It is also enlarged in other somatosensory-dependent
species such as star-nosed moles and nocturnal owl monkeys (Catania & Henry, 2006).
Figure 6.3 The lobes of the brain, and the location of the postcentral gyrus.
Source: Blausen 0101 Brain LateralView.png, CC BY-SA 3.0, BruceBlaus.
Balance
Like touch, the vestibular sense (balance) also involves hair cells. Some are located at the base
of each of three semicircular canals (ducts) in the inner ear, in structures called ampullae
(Figure 6.4). The canals are filled with fluid and are set nearly (but not quite) at right angles to
one another. Because of the slightly off-kilter angles, any rotational acceleration results
in fluid movement in at least two of the canals. That causes hair bending and thus sensing
in at least two planes, enabling the precise neural computation of acceleration information.
Other hair cells are located in fluid-filled cavities called the utricle and saccule, and respond to
vertical and horizontal acceleration (Lundberg, Xu, Thiessen, & Kramer, 2015).
The base of the hair cells synapses onto neurons, which coalesce into the vestibular nerve,
in turn connecting to nuclei in the brain stem (Cronin, Arshad, & Seemungal, 2017). This
pathway produces the vestibular reflex that allows us to keep our eyes fixated on an object
while our heads move. Another pathway terminates, like somatosensation, in SI of the
parietal lobe (D. Schneider, L. Schneider, Claussen, & Kolchev, 2001).
It was once believed that vestibular hair cells originated in the lateral line system of fish. This
system uses hair cells arranged in a line from gills to tail, detecting water currents, the pre-
sence of prey, and possibly the location of sounds. However, the lateral line system and the
inner ear differ in form, development, and function. Therefore, the current view is that both
evolved in parallel from loosely arrayed somatosensory cells, rather than one from the other
(Duncan & Fritzsch, 2012).
The earliest emerging taxa with an identifiable inner ear were the hagfish and lampreys,
placing its origin about 520 million years ago. However, those cartilaginous fish have only
one and two semicircular canals, respectively. The third canal emerged about 430 million
years ago with the evolution of bony fishes (Beisel, Wang-Lundberg, Maklad, &
Fritzsch, 2005).
Figure 6.4 Structures of the inner ear, including the semicircular ducts (canals), utricle, and saccule.
Source: Blausen 0329 EarAnatomy InternalEar.png, CC BY-SA 3.0, BruceBlaus.
A striking aspect of the vestibular apparatus is its extraordinarily restricted size range
across mammalian species. The size ratio of the smallest to largest is less than 1:10, in
contrast to a ratio of possible body lengths of nearly 1:1,000. Possibly its size is constrained
by physical properties such as the inertia of its fluids and the range of hair displacement
in the receptors. When these and other properties are mathematically modeled, a narrow
range of sizes is indeed possible, and the human apparatus is neatly positioned in midrange
(Squires, 2004).
Nevertheless, some size variation is present across species, although its meaning is unclear.
We might expect highly active species like gibbons to have large semicircular canals to
provide more precise acceleration information. However, there is no consistent relationship
between activity/agility and canal size (Kemp & Kirk, 2014; Malinzak, Kay, & Hullar, 2012).
Larger canals may instead benefit species with more acute vision, in order to better stabilize
vision during movement via the vestibular reflex (Kemp & Kirk, 2014).
In agile species, large canals may be less useful than canals oriented 90° to one another.
Across mammalian species, the more the canals are at right angles to each other, the greater
the estimated sensitivity to angular acceleration (Berlin, Kirk, & Rowe, 2013). Even within a
specific group of primates, i.e., strepsirrhines, actual measurements of the speed of head
rotation in a species is correlated to the perpendicularity of its semicircular canals (Malinzak
et al., 2012). The implication is that evolution has reoriented the canals to be more per-
pendicular to one another, in species emphasizing speed and agility. However, the limited
species examined so far do not permit a phylogenetic analysis across primates, let alone
animals more generally.
Hearing
Hearing, or the auditory sense, likewise depends on hair cells to detect mechanical disturbances,
in this case in the air or water medium surrounding the organism. Sound propagates pressure
waves through the medium, and their amplification and detection result in hearing.
However, even at the basic mechanical level, auditory processes are complex. A sound
entering the ear is transformed by the physical structure of the pinna (outer ear), enhancing
middle frequencies in the range of 2,000 to 5,000 Hz. It then impinges on and causes
vibration of the eardrum (tympanic membrane), which transmits the vibration through
three connected ossicles (small bones in the middle ear called the malleus, incus, and stapes) to
the oval window of the inner ear’s cochlea (Figure 6.5).
The sound causes the basilar membrane inside the cochlea to vibrate, and hair cells located
on the membrane detect the vibration (Varin & Petrov, 2009). Thus, before the first neural
response to sound, a series of complex mechanical events takes place. Adding to the com-
plexity, some people can modify the transmission of sound through voluntary control of
middle-ear muscles (Box 6.2).
Figure 6.5 The middle ear.

Source: Blausen 0330 EarAnatomy MiddleEar.png, CC BY-SA 3.0, BruceBlaus.
Box 6.2 Voluntary control over the tensor tympani muscles
Can you tense your middle ears to produce an apparent roaring or rumbling sound? If
so, you are among what is believed to be a minority of individuals who can voluntarily
contract the tensor tympani muscles, one in each ear ( Angeli, Lise, Tabajara, & Maffacioli,
2013). These muscles end in a ligament connected to the midsection of the malleus
( Figure 6.5). Tensing them therefore dampens the movement of the three-ossicle
assemblage that transmits sound from the eardrum to the inner ear.
Contraction of the tensor tympani muscles substantially lowers the perceived
volume of sound, especially sounds of low pitch. The likely advantage is that when
a loud sound is anticipated, the muscles can be tensed, reducing sound transmission
through the middle ear to the inner ear and thus providing protection against physical
damage. Another probable function of the muscles is involuntary, with moment-to-
moment contraction suppressing the self-produced sounds of chewing and speaking
( Angeli et al., 2013).
The tensor tympani muscles have a long evolutionary history. They existed in
mammal-like therapsids ( Panciroli, Schultz, & Luo, 2019) and are characteristic of
mammals generally ( Allin & Hopson, 1992), dating their origins to at least 250 million
years ago. However, early uses of the muscles were probably involuntary in nature,
with voluntary control emerging in some individuals at a much later (but unknown)
date.
If you are not able to voluntarily contract the tensor tympani muscles, you may still
gain a sense of what it is like. Simply yawn widely in a quiet environment. If you hear a
faint trembling sound, it is a low-loudness version of the much more intense
experience resulting from voluntary control.
As we have seen, hair-based mechanoreceptors are very ancient. As with the sense of
balance, auditory hair cells of the inner ear likely evolved from loosely arrayed receptors
of that type. While nonvertebrate chordates have hair cells, they are not located in an ear but
rather in the oral region. Thus, the co-option of hair cells for hearing must have postdated
the chordate emergence 535 million years ago. Probably it was long after, as will become
apparent.
As the primary receptor surface, the basilar membrane is of central interest in evolutionary
analyses. Its initial form was as basilar papillae (a papilla being a rounded projection), one in
each ear, each containing a few hair cells. Coelacanth fish have them, as presumably did their
ancestors about 395 million years ago as a vestibular system modification (Fritzsch, 1987).
However, the lungfish lineage, not the coelacanth lineage, is believed ancestral to tetrapods,
including humans – and lungfish lack basilar papillae. Why do tetrapods share them with
their more distant coelacanth relations, but not with their closer lungfish cousins?
The likely answer is that basilar papillae were inherited from the last common ancestor of
all three groups but were subsequently lost in lungfish. It has been suggested that the
common ancestor was a lobe-finned fish whose papillae were used to assess pressure dif-
ferences between its primitive lungs and its membrane-covered middle ears, allowing the
monitoring of depth (Fritzsch et al., 2013). The shallows-dwelling lungfish presumably had
little need for depth information and so eventually lost the papillae, but not before giving rise
to tetrapod descendants who incorporated them into a more elaborate hearing mechanism.
In tetrapods, a few hair cells became many hair cells. Ultimately the “carpet” of hair cells
became continuous over a lengthened basilar membrane, achieving the mammalian form that
humans have today.
Another evolutionary step coiled the basilar membrane inside a cochlea, packing a max-
imum of membrane surface into minimum space (Figure 6.4). Comparative analyses indicate
that full coiling evolved after monotremes emerged about 195 million years ago, but before
marsupial and placental mammals diverged about 170 million years ago (Manley, 2000; Vater,
Meng, & Fox, 2004). Nevertheless, the earliest known fossil showing coiling only dates back
about 80 million years (Vater et al., 2004).
Frequency selectivity
With these modifications came frequency selectivity, the ability to distinguish between
sounds of differing pitch. Turtles and lizards have little, and birds an intermediate amount,
but mammals including man have substantial selectivity (Manley, 2000). In mammals, se-
lectivity is mostly achieved through organization of the basilar membrane. Hair cells at its
base (nearer to the bones of the middle ear) detect high frequencies, while those near the
membrane’s apex (on the opposite end) detect low frequencies (Breedlove, Watson, &
Rosenzweig, 2010). Frequencies can then be distinguished based on the location at which
hair cells are stimulated.
Lizards lack basilar membrane selectivity but have evolved frequency-related modifications
of the hair cells themselves so that particular cells are more responsive to certain frequencies
than others. Birds also use hair cell modifications, as even mammals do to supplement the use
of location on the basilar membrane (Manley, 2000).
In humans, the modification of vestibular structures for auditory function has been ac-
companied by a substantial shift in the ratio of hair cells to connecting neurons. Vestibular
hair cells show an approximately 5:1 ratio to neurons, indicating some funneling of in-
formation, but auditory hair cells show a remarkable 1:8 ratio – in effect a reverse funneling
or elaboration of processing at the first neural juncture. The elaboration is particularly
pronounced in the case of high-frequency hair cells toward the base of the basilar membrane
(Fritzsch et al., 2002). Indeed, “high end” expansion has occurred over some 350 million
years. Turtles, which are reptiles, may be limited to hearing frequencies under 1000 Hz,
while birds are capable of detecting frequencies up to about 10,000 Hz. Humans, at least
when young, can hear up to about 20,000 Hz, and some other mammals can do so up to
100,000 Hz! (Manley, 2000).
Within primates there is evidence that high-frequency sound detection is related to the
amount of social calling. Species living in larger groups, and therefore employing a wider
variety of social calls, have greater sound sensitivity overall but especially greater high-
frequency sensitivity. This exploits the fact that in the natural environment, background
noise tends to be pitched low. Thus, having social calls pitched at high frequencies makes
them easier to distinguish from the background (Ramsier, Cunningham, Finneran, &
Dominy, 2012).
For many species, another advantage of a higher frequency range is improved sound lo-
calization (Masterton, Heffner, & Ravizza, 1969). Blockage of sound by the head is an
important location cue, and high frequencies (short wavelengths) experience much greater
blockage than low frequencies (long wavelengths). The greater blockage of high frequencies
thus allows a computation of location using differences between the ears in perceived fre-
quency (Breedlove et al., 2010). The same differential blockage is true of other obstacles as
well. That is why we are usually more annoyed by a neighbor’s bass, which tends to pass
through walls, than by their treble, which doesn’t.
However, if an animal’s head is large, there is a more powerful cue than differential
blockage, based on timing. Sound reaches the near ear earlier than the far ear, and the larger
the head, the larger the timing difference. Timing differences tend to be less affected than
frequency differences by other objects in the environment, posing an advantage for animals
large enough to use them. Thus, we should look to large mammals to have a reduced “high
end”, because they have less need for high frequency hearing. That is certainly true of
elephants, which top out at only 11,000 Hz. It is also true of humans, topping out at
20,000 Hz.
Other primates, which tend to be smaller, typically have higher “high ends” than hu-
mans, with nearly all being able to hear over 32,000 Hz. Within land mammals generally
(Heffner, 2004), and primates specifically (Ramsier et al., 2012), evolution appears to have
optimized frequency response to match body size. The range shifts toward higher fre-
quencies in small-bodied species, and toward lower frequencies in large-bodied species.
The between-ear distance and the highest frequency that can be heard show an imperfect
correlation in primates, but is nevertheless substantial (r = −0.63; i.e., with smaller heads
hearing higher frequencies). Even with humans excluded, the correlation remains,
although it is smaller (r = −0.40; Ramsier, Vinyard, & Dominy, 2017).
Although humans have reduced high-frequency hearing compared to our fellow primates,
we do have other unusual auditory abilities. Specifically, we have lower “low ends” than
most primates, being able to routinely detect frequencies close to 30 Hz, or even 20 Hz
under ideal conditions. At our most sensitive frequency we can also hear fainter sounds than
most (Coleman & Ross, 2004; Heffner, 2004).
Origin of the ossicles

Finally, a remarkable evolutionary story concerns the ossicles, the three small bones that
transmit sound through the middle ear. Amphibians, reptiles, and birds have only one ossicle.
Some 385 million years ago, it and the cavity in which it rested were part of the tetrapod
Panderichthys’ breathing apparatus, serviced by breathing holes toward the rear of the skull.
But in Acanthostega 20 million years later, these structures had evolved into a middle ear with
true auditory function (Brazeau & Ahlberg, 2006). Yet with only one ossicle the “high end”
of hearing was limited.
Mammals, on the other hand, have three ossicles. Where did the other two come from?
Astoundingly, instead of evolving anew they were adapted from bones that detached from
the lower jaw, moved away, and reduced in size. As a result, mammals have only one bone in
the lower jaw while other groups have several.
The evolution of the three-ossicle assemblage improved the detection of high fre-
quencies by matching air’s low impedance (the amount of pressure required to produce
a given displacement) to the high impedance of fluid in the inner ear (Manley, 2000;
Masterton et al., 1969). The assemblage was completed after mammals appeared, sometime
after 225 million years ago, and is first known from 195-million-year-old fossils of the tiny
mammal Hadrocodium (Luo, 2001). At some point an eardrum evolved, substantially in-
creasing sound sensitivity. That development occurred independently, through convergent
evolution, in several groups of amniotes including lepidosaurs, archosaurs, and mammals
(Manley & Clack, 2004).
From this discussion it is clear that hearing was a relatively late arrival at the sensory party.
It probably emerged in its most primitive form shortly before basilar papillae were inherited
by coelacanths about 395 million years ago. Subsequently it further evolved in land-based
tetrapods for reasons not the least bit mysterious: Simply put, the thin medium of air
constituted a selective pressure for improved vibration detection. The better the detection of
sounds produced by the movement of predators and prey, the greater the chances of survival.
About 200 million years later, in a common ancestor of marsupial and placental mammals,
hearing became doubly important because it permitted the beginning of acoustic commu-
nications between individuals (Chen & Wiens, 2020).
Evolution’s answer to these problems was the fully developed ear, with an external part
capturing and amplifying airborne sound, a middle portion transmitting it while matching its
impedance to a fluid medium, and an inner portion containing hair cells transducing the
energy into a form detectable by the nervous system. Its highest expression is in mammals,
which have used hair cell modifications, a greatly expanded basilar membrane surface, and an
elaboration of neural processing to extend frequency perception upward.
Smell
As with mechanical sensing, chemical sensing began with simple cellular transport me-
chanisms. Yet today we enjoy a complex ability to smell and to taste. While the olfactory
(smell) and gustatory (taste) sensory systems are closely related in function, more is currently
known about the evolution of the former.
In humans, olfaction begins when a molecule of an odorant binds to the membrane
of a cell in the olfactory epithelium, a layer of neurons lining the upper portion of the nasal
passageway. When binding occurs, a complex chain of reactions is triggered that opens some of
the Na+ channels in the cell membrane. The same scenario plays out as with somatosensation,
with a spike potential propagating throughout the cell and into the axon on its far end.
Taken together, the axons from millions of receptor neurons make up the olfactory nerve,
which travels a very short distance to an olfactory bulb of the brain (Figure 6.6). There is one
bulb on the left and another on the right of the brain’s midline, with an olfactory nerve
connecting to each in ipsilateral (same-sided) fashion. This is the only sensory system which
does not predominantly cross over with each side of the body linked to the opposite side
of the brain.
From the olfactory bulbs, the olfactory tract courses backward in the brain to connect with
cortex on the medial (inner) surface of the temporal lobes. Pathways then run through the
midbrain to connect with prefontal cortex, the forward portion of the frontal lobes (Figure 6.3).
Together these comprise the brain’s olfactory sensory system.
Across at least the first three levels of this system, size is correlated. Examining six species of
small mammals, Srinivasan and Stevens (2019) reported a strong relationship between the size
of the olfactory epithelium and the size of the olfactory bulb. Furthermore, the size of the
olfactory bulb was highly correlated to the size of the medial cortical area it projected to.
Assuming that a larger epithelium requires greater processing, the olfactory system therefore
follows the same “principle of proper mass” that applies to the sense of touch.
During prenatal development, the olfactory epithelium develops from a placode (a spe-
cialized cell cluster), visible as a thickening of the ectoderm (the cells giving rise to external
features like the skin, nails, and hair, and counterintuitively, the brain and nervous system).
Placodes exist for other senses as well, developing into structures of the eye and ear among
others (Steventon, Mayor, & Streit, 2016).
Comparing species suggests that the olfactory placode originated shortly after the
emergence of chordates, but before the emergence of vertebrates. Thus, while it exists
across the full spectrum of vertebrates, its existence in chordates depends on the species.
Amphioxus, considered representative of early ancestral chordates, either shows no evi-
dence at all for placodes (Schlosser, 2017) or the possibility of tiny ones consisting of
only one or two cells (Lacalli, 2004). Furthermore, evidence for either smell or taste in
Figure 6.6 The olfactory bulbs (upper part of I), and olfactory tract (lower part of I) on the underneath side
of the human brain. Also shown is the optic nerve (II) among other numbered cranial nerves.
Source: Blausen 0284 CranialNerves.png, CC BY-SA 3.0, BruceBlaus.
amphioxus is ambiguous at best (Lacalli, 2004). Yet descendants of early-emerging ver-

tebrate lineages such as lampreys do have identifiable olfactory bulbs (Nieuwenhuys,
2002). Haikouella, a transitional form between early chordates and vertebrates, may have
had nostrils and olfactory nerves 530 million years ago, but the evidence is ambiguous
(Mallatt & Chen, 2003). In any case it seems likely that the neural system underlying
olfaction traces its origin to a point after the splitting off of amphioxus’ ancestors but before
the splitting off of those of lampreys, perhaps 530 million years ago.
Olfactory genes
Research on the genes underlying olfaction has yielded new insight into the evolutionary
rise, and in our case fall, of this chemical sense. A few olfactory genes trace back to the early
ancestors of chordates (Niimura, 2012), just before evolution of the olfactory placode.
The evolution of tetrapods was accompanied by a tremendous expansion of olfactory
genes, so that amphibians and terrestrial vertebrates now have several hundreds to thou-
sands of these. The expansion greatly increased the receptors sensitive to airborne odors. In
contrast, coelacanth fish lack airborne odor receptors entirely, and in some whales and seals
whose ancestors shifted from land to sea, their numbers are dramatically reduced. Thus,
there is good reason to believe that it was the transition to land some 370 million years ago,
and the availability of airborne odors, that provided the impetus for olfactory expansion
(Bear, Lassance, Hoekstra, & Datta, 2016).
Today’s terrestrial mammals have an average of about 1,500 olfactory receptor genes. They
are believed to be directly related to the development of specialized odor detectors in the
olfactory epithelium, so that the more genes there are, the larger the range of detectable
odors. Actual behavioral data demonstrating such a relationship are quite limited, however
(Kay, Campbell, Rossie, Colbert, & Rowe, 2004).
A mammalian expansion in olfactory sensitivity is also observable in the form of larger
olfactory bulbs. Larger bulbs service larger numbers of receptors (Heritage, 2014). Because
the bulbs sometimes make impressions on the inside of fossil skulls, their volume can be
measured in extinct species. It is found that a three-stage increase occurred during
the evolution of mammals, all within a 30-million-year span beginning about 225 million
years ago (Rowe, Macrini, & Luo, 2011). Thus, there has been a strong, general mam-
malian trend toward evolving larger olfactory bulbs.
It is all the more striking, then, that the more recent primate trend has been the exact
opposite, toward olfactory bulb reduction. Controlling for overall brain size, the olfactory
bulbs of strepsirrhines are sized about the same as those of close relatives like tree shrews.
But from there on down the line, it was all reduction: The olfactory bulbs got smaller and
smaller, relative to brain size, from haplorhines (splitting off 68 million years ago) to an-
thropoids (66 million years ago) to catarrhines (44 million years ago) to apes (29 million
years ago; Heritage, 2014).
The formation of olfactory pseudogenes

The downgrading of the olfactory system has continued to the present day in modern hu-
mans. Of our olfactory receptor genes, 50% to 60% are nonfunctional pseudogenes, i.e., genes
that have become deactivated because of disruptive mutations. In contrast, only about 20% of
the olfactory receptor genes in mice and dogs are pseudogenes.
Deactivation appears to have accelerated within the last four million years of human
evolution (Gilad, Man, & Glusman, 2005; Go & Niimura, 2008). However, it began
68 million years ago with the strepsirrhine-haplorhine split. Compared to strepsirrhines,
haplorhines have more olfactory pseudogenes in a class designated as TAAR (Eyun, 2019).
It is probably meaningful that this boundary between primate groups is the same as for the
beginning of olfactory bulb reduction. Both may have driven by increasing diurnality.
Sensitivity to odors should be less important in diurnal species with an increased reliance
on vision, as with many haplorhines but few strepsirrhines (Eyun, 2019).
Another phase of deactivation occurred at the platyrrhine-catarrhine divergence 44 million
years ago. Gilad and colleagues have suggested that this phase was related to increased color
vision (Gilad, Wiebe, Przeworski, Lancet, & Pääbo, 2004). They found that pseudogene
formation has been over 10% greater in nonhuman apes and Old World monkeys than
in most New World monkeys (see also Matsui, Go, & Niimura, 2010). However howler
monkeys, a New World species, share the higher rate of pseudogene formation. The sig-
nificance is that among primates, only the apes, Old World monkeys, and howler monkeys
have true trichromatic (three-color) vision. Other New World monkeys do not (Melin,
Khetpal, et al., 2017).
An association between olfactory pseudogene formation and increased color vision
does not prove a causal connection, but it is suggestive. If it is causal, it could be because
improved color vision reduced selection pressure for odor recognition. For example, if
ancestral Old World primates were able to detect ripe fruit more accurately or at a greater
distance using trichromatic vision in place of the sense of smell, that could have rendered
some olfactory receptors unnecessary and led to their loss by the transformation of genes
to pseudogenes.
While that explanation can account for increased pseudogene formation in frugivorous
Old World monkeys, it is unclear how it might account for it in non-frugivorous howler
monkeys. An alternative hypothesis, based on leaves rather than fruit, was advanced by
Dominy and Lucas (2001; Dominy, 2004). They proposed that increased color vision al-
lowed perception of subtle differences between high-protein young leaves and less nutritious
older ones. As the most folivorous of New World monkeys, howler monkeys would have
found that a useful ability, as would many Old World primates during times of fruit shortage.
Indeed, howler monkeys have been found to feed predominantly on young leaves that are
distinguishable from mature leaves on the basis of greater red coloration (Melin, Khetpal,
et al., 2017). Thus, in both Old World primates and howler monkeys, the evolution of
trichromacy presumably allowed the deactivation of many olfactory receptor genes.
But then what accounts for the accelerated deactivation in hominins, who were neither
folivorous nor heavily frugivorous? Gilad and colleagues suggested that human pseudogene
formation was less connected to trichromacy than to the cooking of food, which deactivates
many toxins. The fewer toxins, the fewer olfactory receptors were needed, and so olfactory
receptor genes were converted to pseudogenes (Gilad, Bustamante, Lancet, & Pääbo, 2003).
The cooking hypothesis might account for recent pseudogene formation in hominins.
However, it cannot explain an acceleration in pseudogene formation as far back as four
million years ago, for there is no evidence for the use of fire at that time. A simpler ex-
planation may be that in hominins of that period, increased raw meat consumption was
linked to a reduced dietary reliance on plants and fungi. That also would have reduced the
range of toxins requiring detection, in turn allowing deactivation of the corresponding ol-
factory receptor genes. However, after turning to gustation we will see that toxin-based
explanations run into another problem that is not so easily solved.
Taste
Gustation, or the sense of taste, is a second chemical sense. The receptors are in the form of
cells clustered inside taste buds, in turn located in papillae on the tongue’s surface. The tastes
of sweet, sour, and umami (meaty or savory) are detected much as odors are detected, with
complex molecular binding on the membranes of the cells. Salty and sour tastes, however,
involve simpler mechanisms of ion transport through receptor membranes, with the sodium
(Na+) ions of salt directly transported and with the hydrogen (H+) ions of sour acids
blocking the transport of potassium (K+) ions.
A receptor cell responds to taste by releasing neurotransmitter that crosses a synapse and
activates a neuron in one of three cranial nerves (sensory and motor nerves completely located
in the head), specifically those designated VII, IX, and X (Figure 6.6). These nerves run to
the brainstem, forming a tract that, after a couple of synapses, reaches the somatosensory
cortex in the postcentral gyrus of the parietal lobe (Figure 6.3).
Comparative analyses indicate that all vertebrates including lampreys, but not hagfish, have
taste buds, and that even hagfish have chemically sensitive cells in the mouth area that are
sensitive to tastes (Kirino, Parnes, Hansen, Kiyohara, & Finger, 2013). Thus, the gustatory
system must date from about 520 million years ago with the emergence of ancestral hagfish.
Much of the recent research on gustation’s evolution has focused on bitter tastes, in part
because bitterness characterizes many toxins, and in part because of the discovery of a family
of bitter taste receptor genes designated T2R. The common ancestor of all vertebrates is
reconstructed as having less than 10 T2R genes. Today the number varies widely over species
(Li & Zhang, 2013). Mammals have many more, between 19 and 41 in the species that have
been studied (humans, mice, dogs, cattle, and opossums), while zebrafish, pufferfish, and
chickens have only three or four (Go, 2006).
As in the case of olfaction, there has also been notable transformation to pseudogenes
in some lineages. Although under 10% have been transformed in nonmammalian species,
20% to 40% have been in mammals. Humans occupy the midpoint of the mammalian
range (Go, 2006).
An average level of gustatory pseudogene formation in humans raises questions about
toxin-based explanations, both in gustation and olfaction. If either cooking or raw meat-
eating reduced the toxicity of food, for instance, and that led to olfactory pseudogene for-
mation, there should have been at least as much impetus to convert gustatory genes to
pseudogenes. Thus, the failure to find a higher level of gustatory pseudogenes in humans than
in other mammals casts doubt on the toxin explanation. Unfortunately, it is not yet clear
what alternative can take its place.
Complicating the issue is that when assessed widely across mammalian species, there is a
positive correlation between the amount of vegetable matter in the diet and the number of
T2R bitter taste genes (Li & Zhang, 2013). This is exactly what would be expected of a
toxin-based explanation of pseudogene formation, because carnivores wouldn’t need sensi-
tivity to plant toxins and thus should have fewer functional T2R genes. Herbivores should
have a greatly increased need and thus more functional genes. However, the size of the
correlation is quite modest, r = +0.43, indicating that other unknown factors are in play.
Perhaps if they were known, they would account for the failure to find increased gustatory
pseudogene formation in humans relative to other mammals.
Human ancestors, of course, emerged from a primate background about 7.5 million
years ago. We might expect, therefore, that we would show taste sensitivities similar to
those of our close cousins the chimpanzees. Sweet tastes are a good vehicle for examining
this, because while chimpanzees are omnivorous, their diet is about 55% to 75% fruit, and
they appear to judge fruit from the first bite on the basis of sweetness. When given a
choice between a sugar solution and plain water, chimpanzees are most sensitive in
detecting sucrose, the predominant sugar in many fruits. Fructose, another fruit sugar,
comes in a close second, distantly followed by glucose, maltose, and lactose. Humans
show similar sensitivity for sucrose, but maltose is second (Norlén, Sjöström, Hjelm,
Hård, & Laska, 2019). That is probably meaningful in that maltose is extracted from the
chewing of starches, such as those contained in tubers, a common component of the
human but not chimpanzee diet. Unfortunately it is unclear whether sugar sensitivities are
selected in the evolutionary sense, or merely reflect what is typically available. Perhaps,
for example, both chimpanzees and humans would show increased sensitivity to glucose if
it was a larger part of their diets.
Common trajectories in mechanical and chemical sensing

The near-simultaneous emergence of the vestibular, olfactory, and gustatory systems 520 to
530 million years ago is surely significant. One of the constraints preventing their earlier
appearance was undoubtedly the lack of either a neural net or nervous system prior to the
evolution of cnidarians about 605 million years ago. Nevertheless, the chronological gap of
about 80 million years between the emergence of the neural net and of sensory systems
suggests that an additional constraint was at work, one requiring a long time for evolution to
work around.
What could that constraint have been? A good guess is that it was the limited neural
architecture permitted by early sensory cells. Specifically, the exclusive use of primary sensory
cells, cells with sensors at one end and an axon out the other end, limited the kinds of neural
connections that could be made because the axon prevented the processing of sensory
information prior to its terminus in the central nervous system (CNS). In contrast the
later-evolving secondary sensory cells, in which receptors have a sensory end and a broad sy-
naptic surface on the other end, but no axon (Lacalli, 2004), allowed receptors to form any
number of more immediate connections with other neurons. Such secondary sensory cells
in the form of hair cells emerged with the urochordates and are present in amphioxus,
suggesting an origin somewhat over 535 million years ago.
Although that narrows the gap a bit, it still follows the emergence of neural nets by about
70 million years. Perhaps such a long span of time was required because the evolution and
exploitation of secondary sensory cells involved three interacting components: (a) the loss of
sensory cell axons in at least some receptor types, (b) the substitution of connecting neurons
for those axons, and (c) the organization of the connecting neurons as a system of inputs into
the CNS. A major restructuring may have taken a major interval of time. However, once it
was in place, it was then exploited more or less simultaneously by the emerging vestibular,
olfactory, and gustatory sensory systems.
The vertebrate plan differed from the invertebrate one in important ways that highlight
the extent of the restructuring. Vertebrates came to rely on a large number of relatively
undifferentiated neurons, forming ganglia with the cell bodies inside and axons outside,
leading to a CNS organized inside the skull and vertebrae. In contrast, invertebrates had
relied on a small number of complex neurons, forming ganglia with the cell bodies
outside and axons inside, and a CNS organized around the digestive tract (Rosenzweig,
Breedlove, & Watson, 2005). Thus, vertebrates achieve sensation by adopting a gen-
eralized nervous system structure in which interchangeable sensors plug into a complex
network of simple cells, arranged hierarchically, leading to a central processor. Previously,
invertebrates had achieved sensation by elaborating a few complex neurons using loca-
lized processing.
There is a general understanding that the vertebrate CNS must have evolved from the
simple neural nets possessed by cnidarians, although the intermediate steps remain murky.
This may be because the transitional forms are extinct, and their fossils have not been re-
cognized. In any case, given the scope of the restructuring necessary to overcome limited
invertebrate architecture, the wonder may be that it took “only” 70 to 80 million years to
create the vertebrate computational apparatus.
The other mechanical and chemical senses

Touch, balance, and hearing are not the only mechanical senses. We also use mechanical
sensing to assess joint position and muscle tension, the kinesthetic sense. However, there
appears to be little understanding of its evolution.
Similarly, smell and taste are not the only chemical senses. Receptors in our arteries engage
in chemosensation through sensitivity to changing oxygen and carbon dioxide levels. The
vomeronasal system senses pheromones using receptors in the nasal passages. The system is
vestigial in Old World monkeys and apes, to the point that humans lose their vomeronasal
nerves during fetal development, but it is functional in strepsirrhines, tarsiers, and New
World monkeys. This suggests that the system was largely lost in a common ancestor of Old
World monkeys and apes, in round numbers about 30 million years ago. Evolutionary loss of
the system in primates roughly corresponded in time with the acquisition of three-color
vision, raising the possibility that vomeronasal and olfactory losses had similar causes (Moriya-
Ito, Hayakawa, Suzuki, Hagino-Yamagishi, & Nikaido, 2018). In species with vestigial
vomeronasal systems, the olfactory system has taken over the role of pheromone detection
(Smith, Rossie, & Bhatnagar, 2007).
Conclusion
Our senses have their roots in simple membrane gating mechanisms that relieved excess
pressure and allowed needed nutrients to enter the cell and waste products to leave. These
mechanisms must have existed since the dawn of cells four billion years ago. Today, bacteria
are capable of sophisticated chemical signaling techniques in order to attack a host, to es-
tablish biofilms, or to signal surviving cells to avoid antibiotics. The existence across life
domains of a signaling chemical, rhomboid protein, suggests signaling is ancient. It may even
have been essential for the emergence of unicellular life,
Hair-based mechanoreceptors may have appeared 1.0 to 1.5 billion years ago in choa-
noflagellates, later becoming incorporated into cnidarians as stinging cells. Neurons possibly
evolved from such cells, allowing more coordinated attacks and avoidance of the creature’s
own stings. But however they emerged, neural nets and their support of mechanical sensing
originated a little over 605 million years ago. Hair cells that synapsed onto neurons are
believed to have appeared in early chordates.
Humans have a number of skin-based mechanoreceptors as part of the somatosensory
system. It has two divisions, the medial lemniscal system and the extralemniscal system, with
the former crossing over to the opposite side of the brain and the latter only partially doing
so. Collectively they project to cortical areas SI and SII among others. The size of the cortical
areas serving different body parts varies with the sensitivity of the part.
About 520 million years ago, the vestibular sense appeared in the form of an inner ear,
building on the existence of mechanoreceptors and improving balance and visual tracking
during body movement. Three semicircular canals set nearly at right angles provide our sense
of balance. Two of these were present in ancestral lampreys, but the third only emerged
430 million years ago in bony fishes.
Hearing also emerged as an inner ear faculty, shortly before 395 million years ago. Basilar
papillae, each with a few hair cells, exist in coelacanths. Tetrapods also have them, but not
lungfish, so it appears that while a mutual ancestor of the three groups had them, they were
later lost in lungfish. Eventually, in tetrapods a carpet of hair cells became continuous over a
lengthened basilar membrane. Full coiling of the membrane inside a cochlea occurred about
180 million years ago. Humans largely distinguish sounds of differing frequency by the
locations stimulated on the basilar membrane.
Sounds are localized differently by small-headed and large-headed primate species.
Small-headed species use the blockage of high frequency sounds by the head, allowing a
computation of location by comparing the frequencies perceived by the two ears. Large-
headed species, in contrast, take advantage of a more powerful cue, which is the difference
in the time that a sound arrives at the ears. This is believed to account for the observation
that in general, small-headed animals can hear higher frequencies than large-headed
mammals.
Early tetrapods had only one of the ossicles now found in the mammalian middle ear.
The other two were adapted from bones in the lower jaw. The three together improved
the detection of high frequencies by matching the impedance of air to that of fluid in the
inner ear. The acquisition of the tensor tympani muscles by 250 million years ago likely
allowed the suppression of chewing sounds by damping the movement of one of the
ossicles; today their voluntary contraction reduces sound transmission in anticipation of
loud sounds.
The neural systems involved in chemoreception seem to have evolved about 520 to
530 million years ago after the emergence of the chordates but before that of the
hagfish and lampreys. This is true both of olfaction and gustation. The number of ol-
factory genes increased rapidly after the emergence of tetrapods, who needed to be
sensitive to airborne odors. Mammalian olfactory bulbs also expanded, but in primates
more specifically the olfactory bulbs progressively shrank. Also in humans, many che-
moreception genes have transformed into nonfunctional pseudogenes. Probably this was
at least partially diet-related, although whether it was in compensation for greater reliance
on visual food cues or a decreased need to detect toxins is subject to debate. In humans,
pseudogene formation in gustation has not been nearly as pronounced as that in olfaction,
raising a problem for explanations based on toxins.
The near-simultaneous emergence of the vestibular, olfactory, and gustatory systems
520 to 530 million years ago is surely significant. It was probably due to nervous system
changes allowing unspecialized neurons to connect to synaptic surfaces on sensory receptors,
as opposed to combining neuronal and sensory function in the same cell. Such hierarchical
structure became characteristic of vertebrates.
7 Vision
One of our most important senses does not depend on either mechanical or chemical
stimulation. Although vision involves a chemical reaction, the chemistry involved is internal
to the cell, and stimulation involves light-based rather than mechanical energy transfer. In
this chapter we will first consider how vision began and led to the evolution of eyes. We will
examine how day vision came to sense colors, and how it gave rise to highly sensitive night
vision. We will also see how visual acuity increased in the human ancestral line, producing
improvement in vision that went hand in hand with changes in the brain.
Vision began with single-cell organisms that were neither animal nor plant. Among single-
cell organisms, photomotility (movement in response to light) is widespread and involves
light-absorbing pigments from several chemical classes. These photopigments are embedded in
the cell membrane, in cytoplasm, or even at the base of a flagellum, as in the single-celled
Euglena. In Euglena, rotational movement of the cell causes the light-sensitive pigment to be
shaded by a nearby red eyespot, allowing the direction of light to be determined. This alters
the flagellum’s activity, keeping the organism in an area where light levels are suitable for
photosynthesis (Ogawa et al., 2016).
The evolution of eyes

Metazoan vision involves much greater complexity than that of single-cell organisms.
Initially it may have evolved from a symbiotic relationship, with unicellular organisms
providing primitive vision to multicellular ones. Presumably this was in exchange for pro-
tection or nutrition, much like the relationship leading to the incorporation of mitochondria
into eukaryote cells (Zachar, Szilágyi, Számado, & Szathmáry, 2018). An observation sup-
porting this is that some single-cell dinoflagellates (ocean-dwelling unicellular organisms with
two flagella) possess primitive vision and are common symbionts in cnidarians. Thus, di-
noflagellate genes may have transferred to some ancient cnidarian, making metazoan vision
permanent (Gehring, 2005).
Whether or not that supposition is true, a watershed in the metazoan acquisition of
vision must have been the evolution of multicellular eyes feeding into a nerve net or
nervous system. The first eyes of this type may have appeared among cnidarians, some
of which respond to light by combining pigment cells with neurons. The cubozoans, or
box jellyfish, have fully developed eyes. In fact, each individual has 24 eyes of various
types, including complex lensed eyes arranged in pairs of small and large members,
complete with corneas and retinas. These are connected by a nerve ring with ganglia
(Garm, Oskarsson, & Nilsson, 2011).
What is the purpose of this impressive sensory array? It is known that box jellyfish avoid
obstacles and orient toward light. Unlike most jellyfish, they live near the shore, often in or
near mangrove swamps. Thus, one major function of the eye array is to avoid potential
DOI: 10.4324/9781003137863-9
Vision 115
obstacles that could abrade or destroy delicate tissues (Garm et al., 2011). Supporting this,
experiments in which box jellyfish are placed in cylindrical tanks with striped walls show that
they are more sensitive to vertical than horizontal stripes, as predicted from the vertical nature
of mangrove roots. They even use stripe contrast as a distance indicator, following the
principle that water scatters progressively more light with increasing distance. Accordingly
they particularly avoid high-contrast stripes, because those could be nearby roots. In fact,
with walls of sufficiently contrasting stripes, the animal will hover in the center of the tank,
not making contact with the walls at all (Garm, Hedal, Islin, & Gurska, 2013). Taken to-
gether, these behaviors indicate that jellyfish eyes have an obstacle-avoiding function.
Until recently, a debate raged over whether or not all metazoan eyes descend from a
common origin. One argument in favor of multiple origins (i.e., convergent evolution) is
that eye designs differ radically across species. There are compound eyes with many lenses,
like those of house flies, but there are also homogeneous lens eyes, lensed eyes, mirror
eyes, multiple lens eyes, pinhole eyes, pit eyes, refractive index lens eyes, and two-lens eyes
(Fernald, 2000). That suggests that eyes emerged independently many times in different
lineages, with different designs emerging in response to different needs. For example the
Cambrian species Anomalocaris – a name meaning “strange shrimp”, and a huge one – some
1 to 2 meters (3 to 6 feet) in length – had large compound eyes well suited to a highly
mobile predator operating in well-lit conditions and equipped with a visual brain
(Paterson, García-Bellido, Lee, Brock, Jago, & Edgecombe, 2011). But judging from living
examples, scallops, also originating in the Cambrian, had mirror eyes that served merely as
shadow detectors. These were appropriate to a prey species needing to escape from pre-
dators but possessing little neural architecture (Schwab, 2018). Other kinds of eyes are
believed to have evolved in the human ancestral line, each again meeting a different need
(Box 7.1).
Box 7.1 Intermediary eyes in the human ancestral line
The stages of eye evolution leading up to humans are believed to be understood to a

first approximation ( Figure 7.1) even though supportive evidence is incomplete. In
each instance, an intermediary form improved vision compared to the form
immediately preceding. This satisfied a key requirement – for evolution to proceed,
each product had to leave descendants with a selective advantage over its immediate
predecessor.
In the first stage, a small set of photoreceptors, or even a single receptor, appeared on
the skin and was connected to a nerve net ( Figure 7.1a). Probably first appearing in
cnidarians, the advantage of vision in this instance lay simply in signaling the presence
or absence of light, a distinct advantage over complete blindness ( Picciani et al., 2018).
In the second stage, a depression or folding of the skin created a cavity
( Figure 7.1b). Because the sides of the cavity produced shading of those receptors
not in the direct line of light, this form improved vision by indicating the direction
of a light source, while still being able to signal the presence or absence of light. Eyes
of this type are believed to have evolved in the immediate ancestors of bilateria
( Arendt & Wittbrodt, 2001).
Further contraction of the cavity’s opening, in the third stage, resulted in a pinhole
eye ( Figure 7.1c). Due to optical physics, this created a sharper image, improving
vision by allowing objects to be pictured for the first time. Of course, the direction of
Figure 7.1 Intermediaries in the evolutionary background of the human eye.

Source: Diagram of eye evolution.svg, CC BY-SA 3.0, Matticus78.
Vision 117
light and its presence or absence were still signaled. If you have corrected vision, try
removing your contact lenses or glasses, and peer through a pinhole in a piece of foil to
experience the improved, though dimmer, vision a pinhole provides.
Closure of the eye, so that it was covered by a transparent membrane ( Figure 7.1d),
eliminated entry of water-borne debris, improving vision by minimizing the
obstruction of light. Imaging, directionality, and presence/absence information could
still be extracted. That remained true when a distinct lens evolved ( Figure 7.1e).
Initially this may have been little more than a water-filled sac, but whatever the
structure, it allowed images to come to a better focus on the back of the eye.
Simultaneously the entry for the light pathway became larger, allowing more light to
be gathered than was possible with a pinhole eye. Early vertebrates are believed to have
had paired, lensed eyes ( Bardack, 1991).
In the final form of the eye ( Figure 7.1f), in which a bulging cornea emerged
along with an iris, the image was brought to a precise focus, and the amount of light
entering the eye could be regulated. Pattern vision was much improved, and over a
wider range of light levels. The cornea probably emerged first in early vertebrates as
a protective covering. It provided little optical advantage while its possessors lived in
water, but increasingly did so as the ancestors of tetrapods ventured onto land.
Increasing stiffening of the cornea occurred later in mammals and continued in
humans ( Koudouna et al., 2018).
Thus, in a series of changes, over many millions of years, vision was nearly perfected
in our ancestors. It would require other changes – especially the invention of external
artificial lenses – to perfect it further.
Other indications of the multiple origins of eyes include differences in (a) the organization
of photopigments in the receptors, (b) the receptors’ ion transport channels, and (c) the
development of the eye in embryos. On the other hand, arguing for a common origin is that
all eyes use variations of vitamin A-based photopigments even though other light-sensitive
pigments exist (Fernald, 2000).
The genetic basis of eyes

Fortunately, the acquisition of genetic data has brought greater clarity to the debate over
common origins in vision. It has been found that a set of genes called Pax genes operates
across vertebrate species to direct the development of eyes. One of these, Pax6, appears to
be a “master gene” that controls eye development across its many varieties. Three others
(Pax2, Pax5, and Pax8) appear in mammals, where they influence organ and nervous
system development. Humans have an additional five Pax genes beyond these (Pichaud &
Desplan, 2002).
Significantly given their early evolution, sponges and cnidarians have yet another member
of this gene family, designated PaxB. It was likely the ancestral gene from which other Pax
genes evolved (Kozmik, 2008). Its appearance can be viewed as the first of a number of
important developments in the evolution of vision leading up to primates (Table 7.1).
These observations suggest that the basic control mechanism for eye development was
present 650 million years ago in sponges. In that sense, eyes have a common origin.
However, whether eyes actually evolved in a particular lineage depended on the evolution of
other Pax genes from PaxB. Thus, there has been a substantial amount of convergent
evolution even though all metazoan eyes have some genetic commonality.
Table 7.1 Some important developments in the evolution of vision in the primate ancestral line. mya =
millions of years ago
Characteristic Earliest Example Approximate Date
Pax genes sponges by 650 mya

flavin photopigments sponges? by 650 mya
opsin photopigments cnidarians by 605 mya
paired cup eyes bilaterians by 580 mya
receptor hyperpolarization chordates 535 mya
multiple cone types chordates? 535 mya?
a single, optically reversing eye chordates 535 mya
reappearance of paired eyes chordates 530 mya
lensed, paired eyes vertebrates? by 520 mya
rhodopsin (rods) vertebrates 520 mya
reduction to two cone types early mammals by 215 mya
large corneas primates 68–74 mya
enlarged optic nerve haplorhines 68 mya
well-developed fovea anthropoids 66 mya
corneal reduction anthropoids 66 mya?
recovery of three cone types Old World monkeys 20–44 mya
Many sponges, which have only PaxB, sense light with rings of pigment-containing receptor
cells (Rivera et al., 2012). Some are known to withdraw their oscula (mouth-like openings)
when exposed to light, and their larvae swim directionally in response to light. They are most
sensitive to violet light with a wavelength of 440 nanometers (nm), a response that is consistent
with a class of photopigments called flavins or cryptochromes (called “crypto” because for many
years their identity was unknown; Leys, Cronin, Degnan, & Marshall, 2002).
Perhaps as our legacy from such ancient ancestors, flavin-based photopigment today un-
derlies the human circadian rhythm. This rhythm governs our sensitivity to the 24-hour day,
raising respiration, temperature, and activity levels during the day and lowering them at
night. Light helps set this rhythm and, at least in mammals, does so through visual sensing by
some of the retina’s ganglion cells. Output from the ganglion cells then projects to the
suprachiasmatic nucleus, which controls the circadian rhythm (Do & Yau, 2010).
However, in cnidarians, Pax genes are involved in the production of a different family of
photopigments called opsins. Such genes have been found in cnidarians, but are absent in
sponges (Plachetzki, Degnan, & Oakley, 2007). Consistent with this, peak visual sensitivity in
the cnidarian genus Hydra falls within the range of wavelengths to which opsins respond.
Specifically, hydra are most sensitive to blue-green light, at wavelengths between 480 and
530 nm (Leys et al., 2002).
Putting these observations together, it seems that sponges’ photosensitivity is based on
flavin-based photoreceptors, using a receptor chemistry that is repeated in our regulation of
the circadian rhythm. Receptors based on opsins, which led evolutionarily to complex eyes,
emerged later in cnidarians.
The bilateria appeared soon after cnidarians (see Figure 2.3), about 580 million years ago.
These are animals showing bilateral symmetry, and they include humans. Arendt and
Wittbrodt (2001) concluded that the immediate ancestors of bilateria probably had paired,
pigmented cup-eyes as larvae, each possibly as simple as a single photoreceptor containing a
light-sensitive pigment, with a second pigment close by. The second pigment functioned like
the eyespot in Euglena, providing shading and thus an indication of the directionality of light.
The Pax6 gene and opsin figured into the chemistry of these receptors (Arendt & Wittbrodt,
2001; Nilsson, 2013).
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Chordate and early vertebrate eyes
Early chordates emerged after cnidarians and bilaterians about 535 million years ago, and may
have been similar to today’s amphioxus. Amphioxus larvae have a single Pax-expressed
frontal eye involving a multicellular pigment cup backed by rows of neurons. It is suited to
determining the direction of light, perhaps sufficient to escape predators (Lacalli, 2004, 2018).
The salp, a primitive jelly-like chordate, likewise has a single eye during the solitary phase of
its life (Braun & Stach, 2017). Accordingly, it seems possible that even though bilaterian
ancestors had paired eyes, it was a single eye that passed from chordates to the ancestors of
vertebrates (Lacalli, 2018).
The earliest fossil evidence of eyes among possible vertebrate ancestors is in Haikouella, a
chordate resembling amphioxus. A Cambrian species dating to about 530 million years ago,
several of its fossils unambiguously show paired eyes (Mallatt & Chen, 2003). The basic
structure of the human eye may thus have been set over a half billion years ago during the
chordate-vertebrate transition.
Hagfish, which emerged shortly after, also imply the reappearance of paired eyes.
Living hagfish have two eyes hidden under skin. They are lensless even though lens
placodes are present in embryos, suggesting that the eyes degenerated during evolution.
Consistent with this supposition, hagfish fossils, dating to about 300 million years ago,
show a pair of dark eye spots including small white dots that may represent lenses
(Bardack, 1991; Gabbott et al., 2016). If so, the lenses were subsequently lost. It is
possible that hagfish eyes are now used not for vision, but for circadian rhythm regulation
(Sun et al., 2014).
It is important to note that the ancestral hagfish eye reversed images left-to-right (and up-
to-down). That is because of the geometry involved in its pit structure, as illustrated in
Figure 7.2 (Lamb, Collin, & Pugh, 2007). Whether or not it had a lens did not impact this,
and images would have reversed in either case. However, if present, a lens would have
strongly improved image focusing.
Lampreys, the next group to diverge, definitely have paired, reversing eyes, with lenses
that in the adult produce focused images (Kröger, Gustafsson, & Tuminaite, 2014). This
argues that lenses originated at least 520 million years ago, although they evolved con-
vergently in multiple taxa. Some of the transparent proteins forming the lens are specific to
vertebrates and presumably derive from a common ancestor (Bloemendal et al., 2004).
Color vision
Although the abilities to sense light and to form images from it are fundamental to vision, the
ability to see color is also important to the recognition and evaluation of objects. Some
objects, such as fruit, carry color cues signaling suitability for consumption. Others carry
warnings, as in distinctively colored poisonous snakes, or advertising, as in the colorful
plumage of male birds seeking mates.
In humans, and in all apes and Old World monkeys, normal daytime color vision is ac-
complished with a system of three retinal receptor types called cones. Each type of cone
responds to a broad range of wavelengths and thus colors, but each shows a peak response at a
particular wavelength. Our short-wavelength cones show a peak at 420 nm, in the violet
portion of the spectrum; medium-wavelength cones at 530 nm, a green color; and long-
wavelength cones at 560 nm, a yellow-green. However, these three cone types are often
referred to as “blue”, “green”, and “red” cones, respectively, because each is sensitive to
longer wavelengths as well that include those primary colors. An opsin photopigment is
involved in each.
Figure 7.2 A pit eye. Light from the left projects to the right side of the retina, and vice versa.
Source: Adaptation of Pit eye.svg, CC BY-SA 3.0, Gagea.
It may seem curious to you that we see only a narrow range of wavelengths in an elec-
tromagnetic spectrum running from gamma rays (wavelengths on the order of a thousandth
of a nm), up to the emissions of AC circuits (on the order of 10 to the 15th power nm).
Why is our vision limited to the tiny range of about 400 to 700 nm?
A large part of the answer is that our sensitivity reflects the predominant wavelengths
available on earth’s surface in daytime (Figure 7.3). Above and below visible wavelengths,
there is relatively less to detect. That can only mean that evolution tuned the response of our
cones to the radiation characteristics of our environment.
However, the greater availability of some wavelengths over others only tells part of the
story. While our maximum daytime sensitivity is at 555 nm, fairly close to the availability
peak (Delgado-Bonal & Martín-Torres, 2016), this may not be the case for animals
generally. Bees, for example, show maximum sensitivity at 344 nm, in the ultraviolet range
of light (de Ibarra, Vorobyev, & Menzel, 2014). At first consideration that seems odd in
that most flowers absorb ultraviolet light (de Ibarra, Vorobyev, Brandt, & Giurfa, 2000).
However, some do reflect it, and counterintuitively, ultraviolet reflection specifically
makes red flowers more attractive to bees, most of which lack red color receptors
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Figure 7.3 Solar radiation above the atmosphere (yellow) and at sea level (red).
Source: Solar spectrum en.svg, CC BY-SA 3.0, Nick84.
(Chen, Liu, Sun, & Niu, 2020). Therefore, it may be the need to detect red flowers that
has led to peak sensitivity in the ultraviolet range.
The daytime system is not very sensitive to low levels of light, and so there are additional
receptors called rods which we rely on at night to see dim objects. These receptors are
exquisitely sensitive: A single photon or quantum of light is sufficient to trigger a rod re-
sponse, and 5 to 7 responding rods are sufficient to result in the perception of light (Field &
Sampath, 2017). However, because only one receptor type is involved in dim nighttime
vision, there is virtually no ability to perceive colors unless an object is bright enough to be
sensed by the cones.
The rods and cones are located in the retina, shown in Figure 7.4. The receptors in the
retina operate in backward fashion compared with other senses in two different ways, the first
involving their position and the second involving their effect on neurotransmitters.
First, rods and cones are literally backward in position: The light-capturing ends of the
receptors are oriented away from the light, so that light has to pass through neural ma-
chinery to be captured by photopigment. In fact, as Figure 7.4 illustrates, light must pass
through the ganglion cells, the connecting bipolar cells, and the rod and cone nuclei and cell
bodies before it reaches the light-sensitive disks of the receptors. Fortunately, neurons are
nearly transparent, limiting the absorption and scattering of light. Also, the problem is
minimized in the fovea (the central area of acute vision) because the connecting neurons
bend away from it, taking many of their cell bodies out of the direct light path
(Figure 7.5).
Why the system is arranged this way is an interesting evolutionary question in its own
right. One possibility is that the tight packing of the receptors so severely limits space that the
connecting neurons and major blood vessels cannot both be on the side away from the light.
If so, they must be separated. In that case, it is better to have the mostly transparent con-
necting neurons in the light path and the dark, occluding blood vessels away from it, rather
than the other way around. Even so, except in the fovea, some capillaries are located in front
of the receptors. Normally, we adapt to their presence and are unaware of them. But under
artificial circumstances such as the beaming of a narrow light shaft at the corner of the closed
eye (a cell phone light works well with some fiddling), we may suddenly see the shadow cast
by the network of capillaries.
Figure 7.4 The retina. Light from the bottom must pass through several layers of cells before reaching
the rods and cones.
Source: Adaptation of 1414 Rods and Cones.jpg, CC BY-SA 3.0, OpenStax College.
The second backward aspect of the visual system is that light stimulation slows the flow of
neurotransmitter from the receptors instead of initiating it. When light strikes a receptor,
Na+ channels close, and the receptor hyperpolarizes, becoming negatively charged. This
slows the release of neurotransmitter in a graded manner related to the intensity of the light:
The brighter the light, the less transmitter that is released (Breedlove et al., 2010). This use of
receptor hyperpolarization appears to date back to ancestral urochordates, now exemplified
by sea squirts, some 535 million years ago (Lamb et al., 2007).
Trichromacy
Our possession of three cone types – “blue”, “green”, and “red” – is the origin of the term
trichromacy (the condition of possessing three types of cones). Oddly, trichromacy is not an
advanced evolutionary feature. Genetic analyses indicate that the ancestral state in vertebrates
was tetrachromacy, the possession of four cone types. The “extra” type was tuned to very short
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Figure 7.5 Cross-section of the retina, showing the bending of the nerve fiber layer away from the fovea.
Source: Adaptation of Three Internal chambers of the Eye.png, CC BY-SA 3.0, Holly Fischer, and Retina-OCT800.
png, CC BY 2.0, origin medOCT-group.
wavelengths, allowing sensitivity to ultraviolet light. Consistent with this, some lampreys
have four cone types. Many reptiles, birds, and bony fish do as well, and some species have
cone subtypes, resulting in more than four spectral peaks (Bowmaker & Hunt, 2006).
What happened to reduce the range of color vision in apes and Old World monkeys? The
story is even more dramatic than it appears, because our ancestors passed through an even
tighter bottleneck of only two cone types (dichromacy), meaning that we lost not just one but
two of the original four. This is believed to have occurred in the earliest emerging mammals,
by 215 million years ago (Borges et al., 2018). Today, most mammals continue to have only
two cone types.
These losses were connected to the nocturnal nature of early mammals. Nocturnal animals
generally have fewer cone types than diurnal ones, as well as a smaller cone population
relative to rods. Early mammals lost first one and then a second cone type as their lives
became increasingly dependent on rod-based night vision, following a well-known “use it or
lose it” evolutionary principle. Biological structures require metabolic expenditures to de-
velop and maintain, and so if they fail to convey a compensating selective advantage in
behavior they are selected against. In the case of cones, losing two types reduced metabolic
costs while maintaining visual sensitivity to a range of wavelengths beyond those detected
by rods. The loss was accomplished when random mutations converted cone genes to
pseudogenes, rendering them inactive (Arrese, Hart, Thomas, Beazley, & Shand, 2002;
Bowmaker & Hunt, 2006).
Although the ancestral primate state is somewhat uncertain, it appears more likely than not
that early primates followed the general mammalian pattern and were therefore dichromatic
(Jacobs et al., 2019). That is true of most living lemurs, which, as strepsirrhines, represent the
first branching point of primate phylogeny (see Figure 4.2).
As explained in Chapter 6, Gilad et al. (2004) identified a link between the re-evolution of
trichromacy and olfactory pseudogene formation, with Old World monkeys and the howler
monkey developing three-cone color vision along with a large percentage of olfactory
pseudogenes. With these monkeys’ diurnal lifestyle came the opportunity to judge food
sources at a distance through reddish color cues, whether in fruit or leaves (Melin, Chiou,
et al., 2017). Re-evolving trichromacy, by allowing the detection of ripe fruit through red
coloration, then rendered some olfactory receptors unnecessary and led to their loss.
Interestingly, Madagascar, home to many of the world’s two-cone strepsirrhine species, has
fruit that more often ranges along yellow-blue than along red-green distinctions (Nevo et al.,
2018). That raises a chicken-and-egg question: Did red fruit come first, pressuring toward the
evolution of trichromacy, or did trichromacy come first, pressuring toward the evolution of
red fruit that monkeys would eat, depositing its seeds with ready-made fertilizer? As with
many chicken-and-egg questions, the answer may be “both”, with each ratcheting up
pressure for the other.
Another result of trichromacy’s advantage in detecting reddish food may have been a
preference for red foods. Presented with a choice of artificially dyed sweetbreads, macaques
(which are trichromatic Old World monkeys) choose red ones far more often than they do
green ones. This preference is specific to food itself and does not extend to coverings put
over food (Skalníková, Frynta, Abramjan, Rokyta, & Nekovárova, 2020).
Trichromacy probably became characteristic of a significant number of primate species
only after the New World – Old World monkey split 44 million years ago. The re-creation
of trichromacy in some primates, from an ancestral dichromatic state, beautifully illustrates
the role of chance in evolution, because different primate groups accomplished it in varying
ways with a varying quality of outcome. Old World monkeys and apes accomplished it by
duplicating the gene for the long-wave receptor, and then modifying the duplicate to be-
come sensitive to middle wavelengths (Bowmaker & Hunt, 2006; Davies et al., 2012). The
duplication created different gene sites, so all individuals normally inherit genes for all three
cone types. In Old World monkeys and apes, this solution must have occurred sometime
between 20 and 44 million years ago.
New World monkeys, on the other hand, generally accomplished trichromacy by evolving
different alleles of the same gene and shifting the sensitivity of one toward middle wave-
lengths. Furthermore, the gene involved is located on the X chromosome. This means that
females often show trichromacy, if they inherit differing alleles on their two X chromosomes.
In that case, one X chromosome is randomly inactivated in every cell, resulting in a mosaic of
photoreceptors, with half being the middle-wavelength type and half the long-wavelength
type. That mosaic, together with the third cone type, creates three-color vision. But a price is
paid: Females who inherit the same allele on both X chromosomes are dichromatic. So are all
males, because they have only one X chromosome and therefore only one of the alleles.
Thus, most New World monkeys are only trichromatic as a species, not as all individuals
within the species (Bowmaker & Hunt, 2006; Davies et al., 2012).
The howler monkey, as noted earlier, is exceptional among New World monkeys. After
the evolution of the alternate alleles, it underwent an actual gene duplication, allowing the
two cone variations to become fixed in the population (Surridge, Osorio, & Mundy, 2003).
Molecular-clock estimates place the divergence of howler monkeys from other New World
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monkeys at about 7 million years ago, so the duplication was a fairly recent event (Cortés-
Ortiz et al., 2003; Perelman, et al., 2011).
Night vision
There is strong evidence that the rods used in night vision evolved after cones. Hoke and
Fernald (1997) cited analyses of DNA sequences from humans, chickens, and fish indicating
that rhodopsin, the specific opsin found in rods, emerged prior to divergences among these
groups, but after the appearance of color-sensitive opsins. Furthermore, these researchers
pointed out that rod output converges on cone pathways for transmission from the retina, not
the other way around, and that during gestation, rods develop later than cones. All of these
considerations suggest that rods evolved after cones (Kim et al., 2016).
This conclusion seems surprising because as the superficially less specialized system, in-
volving only one type of receptor, the rod system appears more primitive than the cone
system. Yet in truth, the rod system is highly specialized, having evolved to allow an exquisite
sensitivity to low levels of light. As we have seen, a single photon is sufficient to cause a
response in a rod containing rhodopsin.
The cone-then-rod order makes sense from a broader evolutionary perspective as well.
The largest selective pressure in the history of vision was no doubt toward evolving any
sensitivity to light. Because light is mostly present in the daytime, selective pressure was
maximal for daytime sensitivity, and so it emerged first. Later, more subtle selective pressures
fine-tuned it so that many creatures became sensitive to the low nighttime levels of light.
More recent work on gene sequences agrees with the conclusion that cones came first, and it
dates the cone-rod divergence to a vertebrate common ancestor about 520 million years ago.
Furthermore, it appears that the first of the cone types to evolve was the long-wave (“red”)
type, followed by short-wavelength (“blue”) cones, then medium-wavelength (“green”)
cones, and finally rods (Pisani, Mohun, Harris, McInerny, & Wilkinson, 2006; Wilson, 2007).
The opsins underlying multiple cone types may have emerged in urochordates, perhaps
535 million years ago before the two-round genome duplication described in Chapter 3.
Rhodopsin then emerged at the time of the duplication. However, it is possible that there
was already a dim-light photopigment, perhaps pinopsin, that rhodopsin replaced (Lamb &
Hunt, 2018).
Mechanisms for increasing light sensitivity

Recall that, in humans, a single photon can produce a rod response. Since it is difficult to
improve on perfection, how, then, can we account for the fact that many animals, such as owls,
cats, and tarsiers, have better night vision than humans and, in fact, better night vision than
anthropoids generally? The answer lies in species differences in (a) the light-gathering apparatus
that delivers photons to the retina, (b) the density of rods in the retina, and (c) the neural
machinery collecting information from the retina. The first of these, the light-gathering appa-
ratus, refers largely to the size of the cornea, the transparent bulge in front of the pupil that is one
of the eye’s optical components. Just as a larger telescope lens gathers more light to image faint
details of the cosmos, a larger cornea gathers more light to detect fainter variations in brightness
at night. More photons are delivered to the retina, increasing the number captured by rods.
Large corneas are the rule in primates generally. It is therefore likely that they originated
with early nocturnal primates prior to the emergence of ancestral strepsirrhines about
68 million years ago (Ross & Kirk, 2007). Tarsiers, whose ancestors diverged from our
ancestral line about 66 million years ago, provide a graphic example of enlarged corneas
(see Figure 4.5). Across living primates, there is a strong empirical relationship between
nocturnality on the one hand and corneal size relative to eye diameter on the other.
Anthropoids, including humans, have smaller corneas relative to other primates, attesting to
the existence of later diurnal ancestors (Ross & Kirk, 2007).
A second light-gathering solution is the use of a reflective backing to the retina. The
tapetum lucidum (“silvery carpet”; Land & Nilsson, 2012, p. 139) is the reflective layer behind
the retinas of cats and dogs, responsible for making their eyes shine at night when a beam of
light is directed at them. Photons passing through the retina without being captured are
reflected back, affording a second opportunity for capture. The result is increased night
vision, though at the expense of a slight blurring of the image.
Both of these solutions – large corneas and a tapetum – appear in tawny owls, a nocturnal
species. Significantly, a tapetum is frequently found in the mostly nocturnal strepsirrhines, but
not in the later-evolving tarsiers and anthropoids. Because strepsirrhines emerged early in
primate history, these characteristics provide additional arguments that early primates were
nocturnal (Ross, 2000).
Another improvement on perfection is for nocturnal species to pack a higher density of
rods into the retina. Some owls have close to a million rods per square mm, compared to not
quite 200,000 per square mm in humans (Goodchild, Ghosh, & Martin, 1996; Ross, 2000).
Such tight spacing increases the chances that a photon reaching the retina will be absorbed by
a rod. The tradeoff is that nocturnal species typically have fewer cones, although enough to
support a moderate quality of day vision.
A final improvement lies in how information is collected from the receptors. In the human
fovea – the central area of acute vision in the retina – the ratio of receptors (exclusively cones)
to ganglion cells is between 1:2 and 1:3 (Drasdo, Millican, Katholi, & Curcio, 2007), pro-
viding sharp, detailed day vision. But in the periphery of the visual field (which contains
mostly rods), the convergence onto ganglion cells is as high as 1,000:1 (Goodchild et al.,
1996). Although it makes night vision blurrier, the massive funneling of rod output increases
light sensitivity, since several stimulated rods can signal the same ganglion cell. Nocturnal
animals have even better low-light signaling because they funnel rods into ganglion cells at
even higher ratios. For example, in the nocturnal owl monkey, rod convergence onto
ganglion cells is as much as 16,200:1. By way of comparison, in the diurnal capuchin monkey
(see Figure 4.9), the maximum rod convergence is 6,500:1 (Yamada, Silviera, Perry, &
Franco, 2001).
In the final analysis, the reason why humans do not have better night vision is because our
ancestors did not need it. At night, our ancestors were at rest and hidden, minimizing their
vulnerability to predators. In contrast, as diurnal animals, they needed excellent day vision,
and natural selection pushed them – and us – in that direction instead.
Acuity
The funneling of rods and cones has important consequences for acuity (the ability to resolve
fine visual details). The human fovea’s 1:2 or 1:3 ratio of cones to ganglion cells preserves
high acuity, while the 1,000:1 ratio for human rods does not. Day vision is therefore more
acute than night vision. Similarly, whether a primate species is diurnal or nocturnal has much
to do with their visual acuity. Among New World monkeys, diurnal species have been found
to have two to five times better resolution than nocturnal species (Ross, 2000).
The fovea’s contribution to acuity

The fovea, a relatively recent innovation, is responsible for the high acuity most primates
enjoy relative to other mammals. It consists of a tiny pit in central vision, part of the macula, a
Vision 127
general vertebrate innovation. Among mammals, only anthropoids have well-defined foveas
that are not occluded by blood vessels, a state presumably reached soon after their emergence
about 66 million years ago. The earlier-emerging Strepsirrhini and tarsiers exemplify a
transitional state, with galagos and tarsiers having a shallow or variably expressed fovea with
occluding blood vessels.
Given these observations, it seems safe to conclude that the fovea emerged early in primate
evolution, was partially present in ancestral Strepsirrhini, and was perfected in anthropoids.
Ultimately, visual acuity in the Old World primates and apes has improved until it is two to
three times greater than that in their near relatives, the tree shrews (Ross, 2000).
As you might infer from these differences, substantial disparities exist in the width of the
area of best vision. In the gerbil, it is a bit over 180° – i.e., the visual field shows uniform,
relatively low acuity. In strepsirrhines, it is about 30°, in macaques 4°, and in humans 1.5°,
about the width of our thumbnail held at arm’s length (Heffner (2004). Thus, as acuity
improves across these species, the area of highest acuity decreases.
Furthermore, the width of the area of best vision has influenced auditory localization
thresholds, with narrower areas of best vision accompanying better ability to localize sound.
Thus, within the horizontal plane, gerbils can localize a sound only to within about 28°,
macaques to about 5°, and humans to about 1.5°. Summarizing these results, Heffner (2004)
suggested that selection pressure tuned sound localization to better direct visual attention to
objects. Species with a narrow field of acute vision, like humans, need to judge sound lo-
cation accurately to bring vision to bear on a sound source. Species with a wide field have less
need for this and make do with poorer sound localization.
Eye and brain

Evolutionary changes to the eye might be expected to cause changes in the brain. To ex-
amine this issue, it is first necessary to describe the neural projections from the retina to the
visual cortex.
As we have seen, the rods and cones constitute the visual receptors of the retina. These
synapse onto bipolar cells, which in turn synapse onto ganglion cells. The axons of the
ganglion cells, taken collectively, become the optic nerve, which exits the eye socket through
a small opening in the bone called the optic foramen. The bundle of axons splits at the optic
chiasm, with half crossing the midline and the other half not, in a way that ensures that the
left half of the visual scene (called the left visual field) projects to the right side of the brain,
and vice versa (Figure 7.6). From there most of the axons travel to the lateral geniculate
nucleus (LGN) in the thalamus, where they synapse upon neurons that in turn project to the
primary visual cortex at the rear of the occipital lobe. The primary visual cortex is also known
by a number of alternative names, including V1 (i.e., the first visual area in the brain).
The suggestion that sensory input to the brain might influence its evolution is an old one,
dating at least as far back as a proposal by Grafton Elliot Smith in 1927 (Kirk, 2006). The idea
is simple and logical: If evolution produces changes to the eye, then changes to the brain
should occur as well to accommodate them. In particular, evolution of the fovea and the re-
evolution of trichromacy should have been accompanied by a corresponding increase in the
cortical areas devoted to vision.
Kirk (2006) addressed this issue by examining the size relationship between the optic nerve
and brain in living as well as extinct primates. The size of the optic nerve was measured using
the area of the optic foramen, under the empirically supported assumption that the opening’s
size reflects the size of the nerve bundle passing through it. Because the sizes of the optic
nerve and brain are both highly correlated to body size, the effect of body mass was statis-
tically removed when examining size relationships. These relationships proved substantial:
Figure 7.6 The primary visual pathway, from eye to brain.

Source: Human visual pathway.svg, CC BY-SA 4.0, Miquel Perello Nieto.
Correlations (r) of optic foramen area to brain volume were +.66 in living primates and +.67
in fossil primates, indicating that about 45% of the variation in the brain size of living and
extinct primates is explained by variation in optic nerve size.
Although correlation is not causation, the robustness of these relationships is suggestive. As
Kirk noted, they are consistent with Jerison’s “principle of proper mass”. This principle,
introduced in Chapter 6, holds that there is a relationship between the neural mass devoted to
a function and the amount of processing involved. Those primates relying more on cone
receptors, with increased processing needs, have expanded cortical areas devoted to vision
and thus larger brains.
The most interesting results of the study emerged from the fossil data. Two groups of fossil
primates were included, adapiformes and haplorhines. Of the two, the adapiformes were
more ancient in terms of divergences from the human ancestral line (see Figure 4.2). They
were found to have small optic nerves and small brains—in fact, outside the range of living
primates. In contrast, the haplorhines had relatively large optic nerves and large brains, well
within that range (Kirk, 2006).
These results are telling, for haplorhines with their large brains emerged about 68 million
years ago, while anthropoids with their perfected foveas emerged about 66 million years ago
(Table 4.2). In other words, the evolutionary threshold for larger optic nerves – and bigger
brains – appears to be located at about same place in primate phylogeny as the threshold for a
well-developed fovea. As such the results support a link between acute vision and brain
expansion in primate evolution.
A link between eye and brain continues to the present day. Pearce and Dunbar (2012)
reasoned that in modern populations, eye size (and thus brain size) should be affected by
geographic latitude. At higher latitudes, low-light days are more frequent than at lower
latitudes. Thus, larger eyes should be selected for, because larger eyes have larger corneas that
collect more light. In turn, larger eyes have more ganglion cells, requiring a larger brain to
Vision 129
support visual processing. Pearce and Dunbar therefore examined modern human skulls
curated in a British museum. They found, as predicted, that both eye size and brain
size increased with increases in the geographic latitude of the population that a skull was
drawn from.
Of course acuity-related brain expansion, starting in the Paleocene, was only the first of
several brain expansions in the primate line leading to modern humans. Later ones were to
have other causes.
Conclusion
Vision originated in single-cell organisms in the form of photopigments allowing the or-
ganisms to orient to light. Possibly it was introduced into multicellular animals through
symbiosis, with an initial cooperative relationship with a light-sensitive unicellular organism
eventually becoming genetic.
The first true eyes feeding into neurons were probably in cnidarians, specifically jellyfish.
Today’s jellyfish commonly use pigment cells as a navigation and migration aid, and box
jellyfish use complex lensed eyes to avoid obstacles such as mangrove roots. Along with the
earlier-emerging sponges, cnidarians have a PaxB gene known to play a role in eye devel-
opment. It was probably ancestral to a number of other Pax genes involved in expression of
the eyes, nervous system, and other organs. Thus, the basic control mechanism for eye
development was likely present by 650 million years ago, although the later appearance of
photoreceptor cells and true eyes involved independent evolution in multiple taxa.
Opsin photopigments may originally have been regulated by PaxB. Flavins (crypto-
chromes) are another class of photopigments involved in setting the circadian rhythm via
retinal ganglion cells and the suprachiasmatic nucleus. Ancestral eyes were probably simple
light sensors in early cnidarians, cup eyes in bilaterians and chordates, and paired lensed eyes
in 520 million-year-old vertebrates.
The human visual system is “backward” in two respects. First, the light-capturing end of
the receptors is located away from the light, behind several layers of cells, a design that may
actually minimize the blocking of light, since the cells are nearly transparent while blood
vessels behind the retina are not. Second, when light is detected, receptors hyperpolarize
instead of depolarize. That slows the flow of neurotransmitter, a feature tracing back to
ancestral chordates.
Old World monkeys and apes, including humans, have three retinal cone receptors
with differing wavelength sensitivities, which are used in daylight conditions. The cones
are tuned to the predominant wavelengths available at the earth’s surface. The ancestral
state in vertebrates was four cone types, only two of which were retained in our noc-
turnal mammalian ancestors. A third type, sensitive to middle wavelengths, was regained
independently in New World and Old World monkeys, though in different manners.
This independent development led to individual-level trichromacy in the Old World
branch but in only species-level trichromacy in most New World monkeys. An exception
is the New World howler monkey, which recently evolved species-level trichromacy.
The selection pressure toward trichromacy likely came from red-green distinctions in
food sources.
The cones of the retina are the eye’s original receptors, and rods later evolved from cones.
Rods are sensitive to low levels of light, with a single rod capable of responding to a single
photon, and with sensitivity of the system as a whole increased by substantial funneling of
information from the rods to the cortex. Nocturnal species show more funneling than diurnal
ones, and often have other low-light adaptations, such as a large corneal light-gathering area,
a reflective tapetum lucidum, and a dense packing of rods in the retina.
The difference between the rods and cones in the amount of funneling affects acuity; the
rod system in the periphery of vision has low acuity while the cone system at the macula
has very high acuity. The area of the visual field with the highest acuity has decreased
throughout primate evolution and is only 1.5° in extent in humans. There is a strong
correlation between optic nerve size and brain size in primates, even after correcting for
body size, suggesting that part of the primate brain expansion may be accounted for by
specialization in vision.
8 The origins of motion
As we have seen, the earliest form of sensation allowed substances to pass through cell
membranes. However, early organisms had only a limited ability to exploit such resources,
because they depended on whatever was brought to them by water. Acquiring movement
was a quantum leap in evolution, freeing single-cell life from relative immobility and at least
to some extent from the vagaries of currents. Motion meant that by trial and error, organisms
could shift from areas of scarcity to areas of plenty.
Movement would prove to be a key building block in cognitive evolution. The ability to
shift between locations imposed navigational requirements calling for highly developed
spatial processing abilities. Favored locations needed to be remembered so that movement
could be directed back to them, imposing a need for improved memory. Pattern recognition
processes were required to recognize known locations, and to direct movement toward new
ones affording familiar types of food as well as water and shelter. In humans, movement
also led to bipedalism and a resulting freeing of the hands, allowing the evolution of more
dexterous reaching and grasping – as well as what those imply for tool use and manufacture.
In this chapter, we lay the groundwork for those developments. First, we will look briefly at
the movement of single-cell organisms, before examining early metazoan motion. We then
consider movement innovations introduced in the human line of descent by chordates, tet-
rapods, amniotes, mammals, and primates. The neural mechanisms of movement are con-
sidered, as is the origin of contralateral organization in both the motor and sensory systems.
Single-cell organisms
Locomotion (movement from place to place) originated in early flagellated bacteria. Rotation
of the flagella propelled a bacterium on a straight course. In a beneficial microenvironment,
repeated momentary reversals kept the bacterium in place. Entering a harmful micro-
environment, however, caused abrupt reversal of the rotation, introducing a tumbling
motion and a random change of direction (Machemer, 2001).
Some archaea are also mobile, using structures similar in shape to bacterial flagella.
Although their underlying proteins are similar, there are enough structural differences that
thread-based motility in bacteria and archaea is best thought of as a matter of convergent
evolution. Given a water environment, and the use of proteins during movement, physical
factors like the viscosity of water and the stiffness of proteins led to superficially similar
solutions (Miyata et al., 2020).
As cell sizes increased, gravity posed an increasing challenge, because cells were denser
than water and thus subject to the deadly consequences of sedimentation. In response, eu-
karyote membranes evolved mechanical sensitivity to the force exerted by water displace-
ment on their undersides. This triggered upward swimming, supplemented by photomotility
in light-sensitive organisms (Machemer, 2001).
DOI: 10.4324/9781003137863-10
Metazoa
Early metazoans encountered similar challenges to those faced by single cells, but magnified
by increased mass. Sponge larvae swam, using the beating of cilia on their surface and
end (Leys et al., 2002). Thus, since sponges were the earliest-emerging metazoan phylum
with living representatives, dating to about 650 to 780 million years ago, movement likely
appeared near the outset of animal history. Ctenophores, next to emerge, reached a similar
solution. They used columns of cilia (“combs”) beating in unison, propelling the animal
through water.
Many early metazoans adopted a benthic lifestyle, surrendering to gravity instead of
counteracting it. However, a benthic lifestyle alone could not cope with local variations
in nutrient concentrations. In times of plenty a stationary animal might thrive, but in
times of scarcity there was a strong selective pressure favoring mobility and a seeking of
new resources.
Trace fossils (fossils of behavior as opposed to physical form) depicting trails about 1 mm in
width implicate a surface-grazing form of locomotion in some benthic metazoans of
the Ediacaran (also known as Vendian) period 570 million years ago. Beginning about
545 million years ago, near the onset of the Cambrian period, trails increased to 2.5–5 cm in
width, and burrowing became common at depths up to 5 cm (Chen, Zhou, Yuan, & Xiao,
2019; Collins, Lipps, & Valentine, 2000; Fedonkin, 2003).
Judging from living animals, many of the trails were caused by creeping movements. In
many cases, secreted mucus provided lubrication, and cilia propelled the animal forward.
Some sea anemones, classified as cnidarians, move in this way. They minimize their
“footprint” by keeping only a tiny fraction of their body surface in contact with the seabed,
thus leaving trails only 2–3 mm wide from bodies up to 10 times wider. The secreted mucus
binds the substrate material, leaving a trail that can fossilize. Some flatworms likewise creep
using mucus secretions and cilia, leaving ridged trails resembling some Precambrian trace
fossils (Collins et al., 2000). Cilia-based benthic movement achieves speeds of 1–2 mm/sec,
or .002–.004 miles per hour.
Other animals, however, may have had other means of movement. Yilingia spiciformis,
which resembled a greatly elongated ear of wheat (in fact, spiciformis refers to its spiky ap-
pearance), was a 545-million-year-old species that may have had rows of paired podomeres
(leg segments). If so, their presence presumably implies the use of muscles rather than cilia for
propulsion. A fossil of the creature heading a clearly visible path leaves little doubt that it left
sea-bottom trails up to 2.5 cm in width (Chen et al., 2019). Movement accomplished by
peristaltic waves, similar to that of earthworms, evolved a little later, providing increased
speed as bodies became larger.
Flatworms are notable not just for creeping, but for swimming, involving full-body un-
dulation using muscles. The later-emerging chordates also undulated to swim, but in a more
fish-like fashion due to their stiff notochord. Thus, one possibility is that the cilia used
in swimming by early sponge larvae and ctenophores were adapted in benthic species for
creeping movements, in turn followed by the evolution of muscle tissue that allowed a
reacquisition of swimming.
However, a complication is that muscles may have first evolved for spawning rather than
locomotion purposes. Seipel and Schmid (2005) proposed that an early swimming metazoan
(using flagella or cilia) evolved muscle cells for reproductive purposes. Its descendants then
included benthic bilateria as well as swimming ctenophores and cnidarians. All inherited
muscles, which began to be used for movement. This inheritance became particularly sig-
nificant to the bilateria, whose bottom-dwelling lifestyle led to differentiation between dorsal
(top) and ventral (bottom) sides. That set the stage for the evolution of body segments,
The origins of motion 133
allowing more complex muscle arrangements capable of more complicated movements
(Finnerty, 2005). Yilingia was just such a bilaterian (Chen et al., 2019).
It is indisputable that body segments permitted more complicated movements. In seg-
mented chordates like amphioxus, swimming involves head-to-tail waves of body contrac-
tion controlled by the nerve cord. A swimming rhythm is maintained by alternating cord
segments, a movement pattern that descended to later fish, and from them to tetrapods and
eventually to mammals (Viala, 2006).
Tetrapods
A major feature of the fish-to-tetrapod transition was a shift in emphasis from power supplied
by the forward fins or limbs, in the pectoral region, to the rear ones in the pelvic region
(Boisvert, 2005; Molnar, Hutchinson, Diogo, Clack, & Pierce, 2021). The Panderichthys-
Acanthostega-Ichthyostega evolutionary sequence (Figure 3.3) illustrates the changes. The early
lobe-finned Panderichthys, in the words of Boisvert (2005), was a “front-wheel drive” model,
pairing fish-like undulation of the front part of the body with anchoring pelvic fins.
In contrast, to varying degree Acanthostega and Ichthyostega were “rear-wheel drive”
models. Their appendages shifted toward the side, both front and back; their muscles and
bones enlarged for body support; and the “fin rays” became digits. All limbs lengthened, but
the increase was greater in the rear, where the pelvis also enlarged for increased support.
Thus, the transformation of fins to limbs began in the front, spread to the rear, and ultimately
resulted in transferring power to the rear (Boisvert, 2005).
This shift toward “rear-wheel drive” is significant in light of later locomotor developments
in dinosaurs including birds. But what caused it? The initial “front-wheel drive” state sensibly
used anchoring rear fins to stabilize an undulating body. But once tetrapod ancestors were
free of the mud, what caused the shift toward rear propulsion?
The explanation is that in land animals, the tail became critically important to propulsion.
This is visible in the archosaurs. Ancestors of the crocodilians and dinosaurs, they left ex-
tensive fossils allowing visualization of muscle attachments to bone. All three groups had a
massive muscle, the caudofemoralis longus, located in the tail but connected to the rear limbs.
Although the muscle helped move the tail, biomechanical analysis reveals a more important
opposite function. Specifically, the muscle provided power to the rear limbs, using the heavy
tail as an anchoring point (Gatesy, 1990; Persons & Currie, 2017). Figure 8.1 illustrates this
aspect of its use.
The relevance to tetrapod evolution is that the caudofemoralis longus is a tetrapod
character. It is found even in the early-diverging salamanders, where it does help power
strides (Ashley-Ross, 1994).
Thus, the shift to “rear-wheel drive” involved propulsory use of the tail. It is a beautiful
example of evolution using an existing structure for new purposes, much as jaw bones were
used in the auditory evolution of mammals. The tail, finned and directly propulsive in water,
could no longer be used that way on land. But it could be used indirectly, by anchoring
muscles powering newly evolved rear limbs.
Another tetrapod characteristic was a “step cycle” that moved the limbs in a particular
order. The sides alternated, specifically right hind - right front - left hind - left front. It is
noteworthy that the same step cycle is observed in lobe-finned fishes, indicating that gait (the
cyclical means by which the limbs move the body) traces back to the immediate ancestors of
tetrapods (Prothero, 2007, p. 220).
As a result of these changes, tetrapods enjoyed a leap forward in traveling speed over a solid
surface. One species of salamander, an early-emerging tetrapod lineage, has been clocked
trotting at 0.6 miles per hour (Ashley-Ross, 1994), a 200-fold increase over cilia-based
Figure 8.1 The tail as anchoring point, dorsal view. The caudofemoralis longus is in reddish brown, con-
necting the tail to the femur of a Tyrannosaurus.
Source: Tyrannosaurus muscle mass.png, CC BY-SA 4.0, John R. Hutchinson, Karl T. Bates, Julia Molnar, Vivian Allen,
and Peter J. Makovicky.
movement. However, early tetrapods sprawled severely. Limbs were held outward and the
belly was supported by the ground.
Amniotes and mammals

Several changes occurred en route from the quadrupedal movement of early tetrapods to that
of amniotes and mammals. An ability to partially erect the legs evolved, lifting the body free
of the substrate (Blob, 2001). That ability, similar to what crocodiles do when walking,
existed in Orobates pabsti about 260 million years ago. A 4 kg (9 lb) tetrapod believed to be
very similar to early amniotes, it had a center of gravity nearer the hind legs than the forelegs,
making it a mostly rear-wheel drive model. Yet its limbs, though sprawling, held the body
off the ground. Fossilized trackways known to have been made by the creature show no
evidence of a dragging belly (Nyakatura et al., 2015).
Eventually in mammalian ancestors, limbs further evolved so that body weight was
placed more directly over the legs, reducing mechanical stress. Thus, an erect quadrupedal
posture became the mammalian norm (Blob, 2001). There is some evidence that the
forelimbs could erect earlier than the hindlimbs. But in any case, mammals were soon
brought to an “all-wheel drive” stage, perhaps by 125 to 150 million years ago. Eomaia, the
early eutherian dating from 125 million years ago, had a fully upright posture (Kielan-
Jaworowska & Hurum, 2006).
While these changes were occurring, the limbs evolved from two segments to three,
arranged in a zigzag pattern (see Figure 8.2). Propulsion was provided mostly by the segments
closest to the body, aided by spinal movement. Movement transformed from side-to-side
undulation, to up-and-down oscillation. The shoulders became moveable, while the hin-
dlimbs evolved ankle joints to incorporate lengthened feet. These changes were probably
adaptations for movement over uneven ground, a challenge for small mammals (Fischer,
Schilling, Schmidt, Haarhaus, & Witte, 2002). Once established they then carried over to
later, larger mammals.
Limb changes were accompanied by gait changes. The side alternation of early tetrapods
was a symmetrical gait in that a movement cycle took the same length of time for the forelimb
as for the hindlimb (Ashley-Ross, 1994; Gasc, 2001). Mammals, however, evolved an
asymmetrical gait with different timing cycles for the forelimbs and hindlimbs, resulting
in higher speeds. (Note that in this sense, asymmetry concerns front-back differences, not
Figure 8.2 Three zigzag segments in the hindlimb of a dog.

Source: Adaptation of Dog anatomy lateral skeleton view.jpg, public domain, Wilhelm Ellenberger and Hermann Baum.
left-right differences.) Often both gaits are available, as in the horse’s symmetrical trot but
asymmetrical gallop (Gasc, 2001).
The absence of asymmetrical gaits in early tetrapods was due to their sprawling posture.
Without support directly under the body, sprawling compromises the balance needed for
an asymmetric gait. Even today, sprawling species like salamanders use a symmetrical gait,
nearly always with two or three limbs in contact with the ground even when trotting.
In contrast horses do not sprawl, and their asymmetric gallop can take all four limbs off
the ground simultaneously (Figure 8.3). Although salamanders can support themselves
momentarily on a single leg, this is maintained for only one or two strides before they flop
on their bellies (Ashley-Ross, 1994). Thus, the evolution of a fully upright quadrupedal
posture in mammals, putting weight directly over the legs, was an important milestone in
making fast movement possible.
Primates and hominins

Judging from ankle fossils, at the strepsirrhine-haplorhine divergence (68 million years ago,
see Table 4.2) early primates were adapted for the grasping of vertical supports. From that
it may be assumed that locomotion primarily consisted of vertical climbing and leaping.
Later, as anthropoids, catarrhines, and apes successively emerged, this adaptation was
Figure 8.3 Asymmetrical gallop of a horse, leaving all four limbs off the ground at once (the two leftmost
frames on the bottom).
Source: Muybridge horse gallop.jpg, public domain, Eadweard Muybridge (1830–1904).
progressively lost as walking modes of locomotion re-evolved (Yapuncich, Feng, Dunn,

Seiffert, & Boyer, 2019).
Today, many walking primates have a characteristic quadrupedal stride in which the
forward placement of limbs follows a right hind - left front - left hind - right front series
(Dunham et al., 2019; Granatosky, Tripp, Fabre, & Schmitt, 2016). This diagonal sequen-
cing, of hind and front limbs on opposite sides, differs from most other mammals, which use
the tetrapod’s side-alternating step cycle of right hind - right front - left hind - left front. Also
unlike other mammals, most primates experience more vertical force on their hindlimbs than
on their forelimbs when walking, to the point that the hindlimbs tend to propel while the
forelimbs brake (Hanna, Granatosky, Rana, & Schmitt, 2017). Primates also extend their
forelimbs more than other mammals (Granatosky et al., 2016; Schmitt & Lemelin, 2002).
The fine-branch environment

The reason for these gait modifications is that the first walking primates evolved to occupy an
arboreal, fine-branch environment. Moving along fine branches emphasizes accurately pla-
cing grasping hands. Diagonal sequencing improves balance on narrow supports, and shifting
force to the hind limbs allows the front limbs to better grasp food. Increased extension of the
forelimbs both increases the range of grasping and reduces branch oscillations (Granatosky
et al., 2016; Hanna et al., 2017). Linking primate gait to fine-branch environments is
confirmed by the similar gait of woolly opossums, also a grasping fine-branch quadruped
(Schmitt & Lemelin, 2002).
Other adaptations in many quadrupedal, arboreal primates are unusually mobile limbs,
and large, heavy tails. When an Old World monkey walks on a branch, it uses forearm
rotation to produce slight side-to-side turns of the body to maintain balance. It is probably
easier to do this when there is reduced force over the front limbs relative to the back limbs,
again helping to account for the rearward shifting of force in primates. A second me-
chanism for maintaining balance is rotation of the tail. For example, if the animal starts to
fall to the right, the tail rapidly rotates in that direction. In turn that causes the rear of the
body to make a reactive leftward shift (Larson & Stern, 2006). A mobile tail also facilitates
leaping. Merely lifting it during leaps does much to stabilize the body, reducing pitch error
(Libby et al., 2012).
Diagonal sequencing of stride is widely spread among primates, but tails less so. They are
not just an arboreal feature because baboons, which are terrestrial, have them. Baboons,
however, are subject to open-space predation and often have to run, making the balancing
function of a tail useful even on land. Somewhat more puzzling is why apes do not have tails,
as they are all at least partially arboreal. Indeed, Proconsul lacked a tail even though it is
believed to have been an arboreal quadruped (Larson & Stern, 2006; Mincer & Russo. 2020).
The effect of large bodies?

It is quite probable that body size was involved in the loss of tails on apes. If early apes had
large bodies, tail movement might have had little effect on balance. Once they proved in-
effective, tails would then have been lost as useless appendages (for a similar suggestion, see
Williams & Russo, 2015). Supporting this notion, Proconsul is estimated to have weighed up
to 90 kg (200 pounds), and the contemporaneous Morotopithecus 40 kg (90 lb). Furthermore,
modeling indicates that as tails become smaller fractions of body weight, pitch correction
becomes less effective (Libby et al., 2012). It therefore seems quite plausible that a large-body
stage accounts for tail loss. It may be that a similar body-size explanation accounts for the less
frequent use – though not elimination – of diagonal gaits in the great apes including humans
(Finestone, Brown, Ross, & Pontzer, 2018; Patrick, Noah, & Yang, 2009). Because of their
big bodies, apes do not walk on fine branches and so have less need of a diagonal gait to
reduce branch oscillations.
Primates also differ from most mammals in the nature of their middle-speed gait. Most
mammals trot with an off-the-ground phase, but primates have an “amble” allowing con-
tinuous engagement with the substrate while minimizing vertical oscillations. It has obvious
advantages for moving along branches, although ambling is also available to some large
terrestrial animals such as horses and elephants. An advantage to large animals is reduced
peak forces on the limbs (Schmitt, Cartmill, Griffin, Hanna, & Lemelin, 2006).
So far the description of primate locomotion has emphasized quadrupedalism. That should
be interpreted as including the knuckle walking of gorillas and chimpanzees, involving
folding four fingers into the palm and contacting the ground with the second row of knuckles
(Simpson, Latimer, & Lovejoy, 2018). However, quadrupedalism is deemphasized by the other
nonhuman apes, namely the gibbons, siamangs, and orangutans. All are primarily arboreal.
Gibbons and siamangs are considered true brachiators, while orangutans use a combination of
brachiation, climbing, and clambering, and are sometimes called semi-brachiators.
At this point it is unclear whether ancestral apes were arboreal quadrupeds or brachiators.
Morotopithecus, a 20-million-year-old ape, had a mobile shoulder consistent with brachiation
(MacLatchy, 2004). However, Proconsul, contemporary to Morotopithecus, appears to have
been quadrupedal. Both are plausible candidates for the common ape ancestor.
The hominin background

Only a little clearer is the nature of the last common ancestor of the African apes including
humans. Was that ancestor mostly arboreal, or more of a terrestrial quadruped in the
knuckle-walking style of gorillas and chimpanzees? While knuckle walking as a human
ancestral trait has had its proponents (Young, Capellini, Roach, & Alemseged, 2015), the
preponderance of evidence is against it. For one thing, the detailed knuckle-walking
anatomy of chimpanzees and gorillas differs sufficiently that it likely had independent
origins postdating their (and our) last common ancestor (Kivell & Schmitt, 2009; Lovejoy,
Simpson, White, Asfaw, & Suwa, 2009). Features of the fossil hominin wrist, hand, and
humerus (upper arm bone) have also been interpreted as inconsistent with knuckle walking
(Arias-Martorell, Potau, Bello-Hellegouarch, Pastor, & Pérez-Pérez, 2012; Rein, 2019;
Selby, Simpson, & Lovejoy, 2016).
The shoulder blades of African apes and humans suggest instead that their last common
ancestor was arboreal, and used a cautious, above-branch, clambering style of locomotion.
This was likely somewhat similar to that of today’s howler monkeys, a New World species
(Selby & Lovejoy, 2017).
Similarly, at a later point more specifically in the human ancestral line, the aus-
tralopithecine shoulder joint showed closer affinity to arboreal species such as the orangutan
and New World woolly monkeys, than to gorillas and chimpanzees. The curved fingers of
australopithecines likewise attest to a partially tree-based lifestyle. That has been described as
“generalized arboreality”, and presumably included both above-branch and below-branch
(suspensory) locomotion. It would not, however, have included the kind of agile brachiation
shown by the small-bodied gibbons and siamangs (Arias-Martorell et al., 2015).
Neural mechanisms of movement

In humans, striking effects on movement are often observed after strokes. Specifically, da-
mage to one hemisphere of the brain often impairs movement on the opposite side of the
body. Why does this happen, and how did such a crossover evolve? Before tackling these
questions we first need a basic grounding in the neural mechanisms of movement.
Muscles move because motor neurons synapse directly onto muscle fibers at what is called
the neuromuscular junction (see Figure 8.4). Muscle fibers are actually elongated cells lying
parallel to one another, composed of myofibrils (chains of protein) that contract when sti-
mulated. When enough muscle fibers are stimulated, the muscle as a whole contracts.
Motor neurons originate either in the spinal cord or in cranial nerve nuclei. A number of
motor actions are initiated as reflexes at these levels, without brain input. For example, stepping
on a sharp object in bare feet elicits a rapid foot withdrawal because the sensation triggers a
multisynaptic pathway looping from the foot to the spinal cord and back to the foot.
Most complex movements, however, require direct intervention by the brain. These are
mediated by two major sets of pathways extending down the spinal cord from various levels
of the brain including the cerebral cortex. One is the corticospinal tract, also known as the
pyramidal or dorsolateral tract. This system is a contralateral one: In other words, it shows
complete crossover from one side of the brain to the opposite side of the body. The tract
originates in the precentral gyrus, or primary motor cortex, the rearmost strip of the frontal
lobe (see Figure 6.3). Moving downward, most of its crossover occurs at the level of the
Figure 8.4 The neuromuscular junction. 1 = axon, 2 = synaptic junction, 3 = muscle fiber, 4 = myofibrils.
Source: Synapse diag3.png, CC BY-SA 3.0, Dake.
medulla. The tract continues to descend to a segment of the spinal cord, where it synapses
with motor neurons that travel to the muscles.
Damage to the primary motor cortex therefore affects movement on the opposite side of
the body due to the crossover. Because the tract largely controls movement of the distal
(farther from the core) musculature, damage to it is more likely to affect the hands and lower
limbs than it is the trunk muscles.
The other tract is called the extrapyramidal tract, although there are actually several distinct
pathways. What they have in common is that crossover is only partial. Thus, the pathways
from the brain divide, with part going down the same side, and part crossing over to the
opposite side. This allows either side of the brain to control both sides of the body. However,
unlike the corticospinal tract, the extrapyramidal tract largely innervates proximal (nearer to
the core) musculature such as trunk muscles that maintain posture.
With this background, we can easily address the question of why damage to one hemi-
sphere often impacts movement on the opposite side of the body. What is observed in such
cases is the effect of the corticospinal system, which crosses over. With one hemisphere
damaged, cortical control of the opposite distal musculature may be disrupted. Proximal
musculature is much less affected because the bilateral (two-sided) extrapyramidal system
allows those muscles to be controlled by the undamaged hemisphere.
That answers the “why” question of opposite-side effects of hemispheric damage. But how
did such a crossover evolve? That is both more interesting and more difficult to answer.
The origin of contralateral organization

To begin with, it is important to recognize how fundamental crossover is in the nervous
system. It is not merely a motor phenomenon. As we saw in the previous chapter, when we
fixate vision on a point in space, everything to the left of that point projects to the right
hemisphere of the brain, and vice versa. Auditory input and a touch to the skin largely
project to the contralateral hemisphere as well, though not as completely.
At first glance this arrangement seems nonsensical, producing an unnecessarily complicated
architecture requiring neurons to pass from one side of the body to the other on the way to
or from the cortex. What accounts for this crossover of sensory and motor projections?
Cajal’s proposal
The famous neurophysiologist Santiago Ramón y Cajal (1852–1934) argued that the origin
of crossover was the reversal of images by the eyes, a simple optical property (Vulliemoz,
Raineteau, & Jabaudon, 2005). Given that images reverse, the problem faced by the nervous
system is how to achieve a continuous representation in the brain. According to Cajal, an
uncrossed system results in discontinuity, as at the bottom of Figure 8.5 where the word
“BEAR” is represented across the cerebral hemispheres as “ARBE”. A crossed system, in
contrast, achieves continuity and reproduces the two halves of the visual scene in the correct
order (top of the figure). When the two sides of the midline are bound together using the
between-hemisphere connections of the corpus callosum, a fully coherent representation is
achieved and “BEAR” is represented as “BEAR”.
Cajal assumed that with the left side of the visual world represented in the right
hemisphere, and vice versa, the other senses would need to be arranged similarly. That
would allow a coherent global representation of the world in which all input from one
side would be integrated in the same hemisphere. The motor system would also need to
follow suit, to control responses on the same side on which stimulation is received
(Vulliemoz et al., 2005).
Figure 8.5 Image continuity in a crossed system (top), and discontinuity in an uncrossed system (bottom).
The two curved segments at the bottom of each diagram represent the left and right cerebral
hemispheres.
A problem with Cajal’s proposal

Cajal’s explanation is elegant, and it captures something important about crossover: Potentially,
the simple optical properties of an image-reversing eye provide the seeds for contralateral
organization. However, his proposal depends on interconnected hemispheres to make visual
continuity relevant by knitting together the two sides of the midline. That did not occur until
long after reversing eyes evolved. Indeed, the corpus callosum, the primary cross-hemisphere
structure connecting the hemispheres, was a relatively late innovation. It first appeared in
eutherians, dating its origin at about 170 million years ago (Suárez, Gobius, & Richards, 2014).
In contrast, the reversing eye is quite ancient, tracing at least as far back as chordates in our
ancestral line and therefore well over 500 million years ago. Amphioxus, the living re-
presentative of primitive chordates, has a visual system that has been interpreted as homologous
(traceable from common origins) to that of vertebrates. Thus, its single frontal eye has in-
terneurons (small laterally connecting neurons) as well as what appear to be the equivalents of
bipolar and ganglion cells, all found later in vertebrates (Butler, 2000; Lacalli, 1996).
On this basis it seems likely that vertebrates descend from an ancestral condition similar to
that of amphioxus larvae. The startling aspect of that condition, of course, is that there was
only one eye. Indeed, it has been suggested that the condition may possibly represent “a
primitive undivided stage in eye evolution” (Lacalli, 1996, p. 244).
In recent decades the genetics of eye development has come to be better understood, in
particular the means by which one eye becomes two in vertebrates. During development a
single eye patch first emerges under control of the Pax6 gene, but a genetically controlled
signaling molecule whimsically named “sonic hedgehog” causes it to split, leading to the
development of paired eyes. Interrupting sonic hedgehog can lead to the failure of this
process and the development of a single “cyclopic” eye in minnows, tadpoles, and mice
(Butler, 2000; Chow & Lang, 2001). Amphioxus seems stuck at this developmental stage.
Figure 8.6 Illustration of the proposed origin of the visual crossover in paired reversing eyes. Left: Single eye,
with same-side projection of each retinal half. Right: Paired eyes, following the same projection
pattern.
The seed of contralateral representation that was proposed by Cajal is present in the single
amphioxus eye. The visual receptors are arranged in cup form and are shaded by the cup’s
sides (Lacalli, 1996). The eye is therefore a reversing eye, as in Figure 7.2. Neural output
from the receptors largely project back along the same side (although receptors at the midline
of the eye project to both sides; Lacalli, 1996). As a result, while the neural pathways
themselves do not cross over, representation of the visual world is mostly contralateral
because of image reversal (Figure 8.6, left).
A modified proposal
There have been other proposals for the origin of crossover, e.g., that it resulted from a
physical “twist” that occurred in a proposed flatfish-like ancestor of vertebrates (de Lussanet
& Osse, 2010). However, Cajal’s reversing eye seems compelling as a proposed point of
origin. It is proposed here that the emergence of paired eyes, which occurred no later than
ancestral hagfish (Chapter 7), is what resulted in the full crossover of neural representation
illustrated on the right side of Figure 8.6.
Evolutionarily, what is proposed is the following. First, a single reversing eye appeared.
At roughly the same time, a partial motor crossover evolved in order to coordinate the
two sides of an undulating tail. Contraction on one side of that midline structure needed
to be paired with relaxation on the other, creating a need for motor commands to affect
muscles on both sides. Partial crossover probably also allowed the use of timed opposite
contractions, allowing the tail to cyclically flip back and forth (Lacalli & Kelly, 2003).
Notice, though, that the effect of a partial motor crossover is to allow both sides of the
body to be moved by either side of the nervous system. This is the arrangement of the
extrapyramidal tract.
Next, the eye duplicated, an evolutionary success because the eyes provided somewhat
differing views and thus improved surveillance. The duplicated eyes, it is proposed, simply
followed the same projection pattern of the single eye: The left side of each eye back along
the left side, and the right side of each back along the right side. The result was essentially the
modern crossover of projections (Figure 8.6, right).
Given this simple beginning, the remaining puzzle pieces fall into place much as Cajal
proposed. Because each half of the visual world was mapped onto the opposite side of the
nervous system, selection also favored crossover in the auditory and tactile sensory modalities.
That kept the global view of the world consistent. As motor responses came to be made not
just by midline structures but by distal ones away from the midline (e.g., fins and limbs),
increasing crossover continued to be favored in order to bring the motor and sensory worlds
into congruence. Therefore, the corticospinal tract is contralateral.
Finally, paired eyes and crossover led to a divided brain with left and right cerebral
hemispheres. Both were present in vertebrates as an early evolutionary emergence after
chordates (Kapoor & Khanna, 2004), before the evolution of bony fish (Vigouroux et al.,
2020) and at least as early as the evolution of lampreys (Pombal, Álvarez-Otero, Pérez-
Fernández, Solveira, & Megías, 2011; Suryanarayana, Robertson, Wallén, & Grillner, 2017).
Thus, it is proposed that a cascade of mutually reinforcing evolutionary changes caused
crossover to become a primary organizing principle of the vertebrate world, all of it traceable
to a reversing eye.
Conclusion
Movement originated with flagellum-propelled bacteria. However, early free-swimming
metazoa used cilia for thrust. Cilia were probably also used by benthic species for grazing,
made possible by lubricating mucus secretions. Trace fossils indicate this type of locomotion
existed about 570 million years ago.
Later muscles powered movement, by moving leg segments or by causing peristaltic waves
that pulled animals forward. However, it is possible that muscles were initially used for
spawning rather than locomotion. Hox gene-based segmentation of the body beginning with
chordates allowed swimming by way of head-to-tail waves of body contraction.
The transformation from fish to tetrapods produced a shift in power from the pectoral fins
to the rear limbs. Once bodies could clear the substrate, the rear limbs continued to power
strides because of their anchoring to the tail. One tetrapod characteristic was a “step cycle”
that moved the limbs in a particular order, the cycle having its origin in lobe-finned fishes.
Early amniotes had a sprawling posture that nevertheless held their bellies off the ground.
About 125 to 150 million years ago the sprawl gave way to an erect posture in mammals,
spreading power more evenly between the limbs. Limbs evolved a third segment, forming
a zigzag pattern that produced an up-and-down rather than side-to-side oscillation, an
adaptation to uneven ground. A symmetric gait characterized by the simple alternation of
sides, transformed to asymmetrical walking and trotting in which forelimbs and hindlimbs
had different timing cycles. An example is the horse’s gallop, which can leave all four limbs
off the ground.
Judging from ankle fossils, early primates were vertical climbers and leapers. Later ones,
however, evolved a quadrupedal stride with diagonal sequencing and forearm extension,
both of which are adaptations for an arboreal, fine-branch environment. In many species
heavy tails help maintain balance by producing a counterrotational shift of the body when
moved to one side. Lifting the tail also helps stabilize the body during leaps. However, apes
lost their tails, probably because they passed through a large-body phase of evolution in
which a counterbalancing tail was of little help. Primates including apes also have an “amble”
that allows continuous engagement with the substrate.
Knuckle walking, characteristic of gorillas and chimpanzees, has been thought by some a
human ancestral trait. More recent evidence, however, has found features of the hominin wrist
and humerus to be inconsistent with knuckle walking. More likely our hominin ancestors
engaged in “generalized arboreality” with both above-branch and below-branch locomotion.
One prominent feature of the neurology of movement is that control of distal
movement crosses over, with the left hemisphere controlling the right limbs and vice
versa. This may have occurred to make motor control congruent with sensory re-
presentation. That also largely crosses over, an arrangement that probably traces to optical
image reversal by the eyes. It is proposed that neuronal arrangement in the single-eyed
amphioxus, in which each half of the retina projects straight back along the left and right
sides, was simply duplicated when the eyes duplicated, producing true crossover of neural
representation. Other senses followed crossover schemes to produce consistency in the
global view of the world.
9 Bipedalism
At the onset of the hominin clade, primate quadrupedalism gave way to bipedalism. How
and why this occurred have always been central issues in human paleontology. Many sub-
sequent developments depended on a bipedal stance, for it freed the hands. In turn our hands
manufactured tools as well as the other multivaried artifacts of culture, giving form to human
cognition.
As we have seen, the cranium of “Toumai”, the 7-million-year old hominin close to the
chimpanzee-human divergence, shows signs of bipedalism in a downward-opening, rela-
tively centered foramen magnum. In a recent report (still undergoing critical review as of this
writing), a number of bipedal features have also been identified in a femur associated with
Toumai, and thought to be from the same Sahelanthropus tchadensis species. Among others,
the reported features include a hominin-like orientation and compression of the femoral neck
(although nearly all of it is missing), a flattening that in other hominins indicates that the neck
was a long one; and a pattern of localized thickening and thinning of the shaft that is human-
like and not ape-like. Its describers concluded that Sahelanthropus was a biped, though one
capable of careful climbing (Guy et al., 2020).
However, some doubt remains because of the curvature of the femur. Guy et al. re-
ported their impression that the curvature resembles that of more certain bipeds like
Australopithecus and Orrorin. Yet actual measurements of the curvature suggest greater
similarity to apes, leading one team of researchers to conclude that it was not an
habitual biped and possibly not even a hominin (Macchiarelli, Bergeret-Medina, Marchi,
& Wood, 2020).
In contrast Orrorin tugenensis, a million years younger, leaves little doubt as to its mode of
locomotion because of a number of bipedal features including a long femoral neck (Almécija
et al., 2013; Kuperavage, Pokrajac, Chavanaves, & Eckhardt, 2018). Certainly by 3.4 million
years ago, the strongly bipedal characteristics of Australopithecus afarensis can leave no doubt
that full bipedalism had evolved (Ward, Kimbel, & Johanson, 2011).
The most parsimonious conclusion is that bipedalism was present in some form since the
onset of the human clade. Indeed, it may very well define it. If so, we need to know why it
began, how it evolved, and what consequences came of it.
The causes of bipedalism

When considering the possible causes of hominin bipedalism, the influence of earlier forms of
primate locomotion should not be overlooked. The primate extension of arms and rearward
shift of weight can be viewed as preadaptations for later bipedal postures. In effect, with the
hands freed of a major support role and body weight predominantly on the legs, only limited
adaptations were needed to stand up. Of course the question is why we took up habitual
DOI: 10.4324/9781003137863-11
Bipedalism 145
bipedalism, while other apes did not. This will be a good question to keep in mind as we
consider several possible causes of our bipedalism.
Efficiency
Could it have evolved because it was a more efficient means of locomotion? For many years
it was assumed, based on running, that it is energetically inferior to quadrupedalism. For
example, Alexander (1992) reported that when running, humans are less efficient than a
typical mammal of similar mass. It was concluded, therefore, that increased efficiency could
not be bipedalism’s cause.
Analyses since then have modified that conclusion. Steudel-Numbers (2001) found that at
three miles per hour, human walking saves 20% of the energy used by a typical similar-sized
mammal. Nevertheless Steudel-Numbers discounted this difference because a third of
similar-sized quadrupedal mammals proved more efficient than humans, and because early
bipedal hominins would have walked less efficiently than modern ones. Halsey and White
(2012) took a similar stance. They reported that walking is more efficient (and running less
efficient) in humans than in the average similarly sized mammal, but deemphasized the
outcome because humans fell within the overall range of comparison species.
However, Leonard and Robertson (1997) correctly pointed out that the proper com-
parison group is not mammals generally, but apes specifically. Thus, the walking efficiency of
the human ape need only have exceeded that of its ancestors for increased efficiency to help
explain bipedalism’s appearance. As it happens, apes are notably inefficient walkers: The
human energy savings over their quadrupedalism falls in the astounding range of 50% to 75%
(Leonard & Robertson, 1997; Sockol, Raichlen, & Pontzer, 2007).
Also under reconsideration is the assumption that early bipeds were notably less efficient
walkers than modern ones. Initially Australopithecus afarensis was thought to have moved with
a shuffling bipedal gait (Hunt, 1994), or even quadrupedally like a baboon but with occa-
sional bipedalism (Wood, 1992). Further research soon indicated, however, that afarensis was
a habitual biped (Ward, 2002). A notable afarensis feature is a long femoral neck (Figure 9.1),
permitting an angling-in of the thighs to place body weight directly over the knees in a
bipedal stance (Lovejoy, Meindl, Ohman, Heiple, & White, 2002). Chimpanzees have
a short neck, while a long neck is characteristic of the australopithecines and early Homo
species (Marchi et al., 2017).
Biomechanical simulations indicate that afarensis was capable of walking efficiently in an
upright position (Wang & Crompton, 2004). Furthermore, it was most efficient at a speed of
1.0 m/sec (2.2 mi/hr), matching the speed inferred from adult footprint trails at Laetoli (see
Figure 5.6). Although afarensis was slower than modern humans, who walk most efficiently at
1.5 m/sec (3.4 mi/hr), it was also shorter. But in any case, its gait was notably more efficient
than chimpanzee quadrupedalism, allowing the conclusion that it was “a fully competent
biped” (Sellers, Cain, Wang, & Crompton, 2005, p. 439).
This conclusion is reinforced by close analysis of Australopithecus africanus femurs. The un-
apelike greater thickness of cortex on the inferior as opposed to superior surface of the
femoral neck is consistent with bipedalism. However, the femoral neck angle was reduced
compared to modern humans, probably implying some side-to-side rocking, and thus a
somewhat less efficient gait (Ruff & Higgins, 2013).
One problem with australopithecine efficiency analyses, however, is that they focus on a
period postdating the appearance of bipedalism by some three to five million years. The
limited fossil remains do not allow a determination of whether bipedalism in its earliest form
was notably more efficient than ape quadrupedalism. Thus, the efficiency issue cannot be
fully addressed until more extensive fossils are found of the earliest hominin species.
Figure 9.1 Femur with long femoral neck (top) in Australopithecus afarensis.
Source: Adaptation of Lucy blackbg.jpg, CC BY-SA 3.0, 120.
Climate change, foraging, and thermoregulation

Several other reasons for adopting bipedalism have been proposed. One possibility is that
hominins were pressured toward it by climate change that resulted in more widely spaced
food trees. With longer travelling distances, bipedal apes may have been advantaged over
quadrupedal ones (Stanford, 2003).
An alternative explanation emphasizes foraging behaviors. Perhaps bipedalism improved
the ability to reach fruit on overhanging branches. In woodland and forest, chimpanzees
naturally adopt bipedal postures when foraging from tree limbs (Hunt, 1994; Stanford, 2006).
Furthermore, experimental presentation of elevated food sacks to chimpanzees increases
bipedal postures, though of an “assisted” type in which the legs support most of the body
weight with minor assistance from other body parts (Videan & McGrew, 2002). It thus seems
plausible that bipedal stances improve foraging.
Another possibility is that upright posture improved thermoregulation by exposing less
of the body to direct sun (Dávid-Barrett & Dunbar, 2016). Modeling shows a favorable
Bipedalism 147
thermal balance for bipedalism compared to quadrupedalism. It even suggests that thermal
considerations may have played a role in out-of-Africa migration. Unable to cope with the
heat of low coastal altitudes, australopithecines might not have been able to leave at all,
making Homo ergaster, a more efficient biped, the first migrating species (Dávid-Barrett &
Dunbar, 2016).
Carrying
A final possibility is that a need to carry objects produced a selective pressure toward
bipedalism. One version of the hypothesis is that bipedalism allowed mothers to carry their
infants (Hodges, 2017). Others, however, emphasize the role of inanimate objects. For
example, chimpanzees carry rocks to nut trees, at distances up to several hundred meters,
where they are used as hammers and anvils to crack tough shells (Mercader, Panger, &
Boesch, 2002).
Even food itself is carried. Providing captive chimpanzees with piles of fruit results in
upper limb carries using unassisted bipedality, i.e., with full weight on the legs (Videan &
McGrew, 2002). If nuts are provided requiring a hammer stone, both are carried bipedally
(Carvalho et al., 2012). Thus, prized food items are carried sufficiently far that they can be
consumed without interference.
Although the carrying explanation of bipedalism is intuitively appealing, it is not entirely
problem-free. First, early hand-carried loads must have been very restricted in weight.
Simulations suggest that loads were limited to 50% of upper limb mass in Australopithecus
afarensis, in contrast to 200%-300% in Homo ergaster and nearly 800% in modern humans
(Wang & Crompton, 2004). In species preceding afarensis, hand-carriable loads may have
been even more limited. A second problem with the carrying explanation is that it seems
most applicable to open savanna, where widely-spaced trees might have required the
transport of stones from one to another. Yet the earliest known hominin, “Toumai”, lived in
a mosaic environment consisting not only of savanna, but also woodland, grassland, and forest
(Brunet et al., 2004).
A closer look, however, suggests these may not be problems for the carrying explanation
so much as they are important features of it. First, perhaps only light loads were involved,
well within the severe weight restriction on hand carrying. Such light loads might have
included simple vegetation-based tools and hunting weapons. Second, a mosaic environment
may have necessitated carrying items into areas where they were otherwise unavailable. For
example, a spear might be difficult to acquire in grassland. Thus, a mosaic environment may
itself have been an important influence on the adoption of bipedalism.
Chimpanzees certainly hunt small animals for meat, so it seems reasonable to assume that
the last chimpanzee-human common ancestor did as well. Chimpanzees encountering a tree
with red colobus monkeys follow a strategy in which several individuals drive monkeys into
part of the tree crown or to the ground where they can be caught. Once caught the monkey
is killed either with a bite to the cranium using the canine teeth or by flailing it against the
ground or a limb. Adult males are the primary hunters, and they succeed the majority of
the time (Gilby et al., 2017; Stanford, 1996; Watts & Mitani, 2002). Other encounters are
more spontaneous, as when a young pig or antelope is encountered and quickly grabbed. The
annual caloric intake from hunting is not insubstantial, by one estimate approaching 8%
to 9% of total calories (Stanford, 1996).
Of course this style of hunting is mostly uninformative with respect to a carrying ex-
planation of bipedalism, since no weapons are involved. Recently, however, a second type of
hunt has been observed that is more directly relevant. Chimpanzees in Senegal have been
found to prepare branches for use as spears, involving breaking off a living branch, stripping it
of leaves and twigs, and modifying one end to sharpen it. It is then used to forcefully probe
tree holes for galagos sleeping during the day (Pruetz et al., 2015). It seems quite possible that
early hominins engaged in similar behavior, advantaging the carrying of a prepared spear
from one place to another.
Hominin vegetation-based weapons would be consistent with weight-limited carries in
that neither spears nor clubs need be heavy. They are also consistent with an observed
shrinkage of canines, the fang-like teeth used by chimpanzees in aggressive encounters in-
cluding hunting. Canine reduction occurred as far back as seven million years ago in
“Toumai” (Brunet et al., 2004). If weapons were used, they may have eliminated the need
for large canines, leading to their reduction according to the “use it or lose it” principle.
A hunting-carrying contribution to the evolution of bipedalism is thus consistent with a
wide range of evidence, including observations of hunting in chimpanzees; a variable,
mosaic habitat; limitations in upper limb strength; and reductions in canine size. However,
it remains controversial. Some resistance to the idea can be accounted for by the absence of
stone tools, including weapon points, until later when bipedalism was highly advanced.
The rejoinder, of course, is that the earliest weapons would have been crafted as chim-
panzees craft them, from perishable materials such as sticks. These would likely not be
preserved in the fossil record.
Why aren’t other apes bipedal?

Combining all of these considerations, it seems likely that bipedalism originated in behavior
already present in the chimpanzee-human common ancestor. That ancestor was probably
capable of bipedal postures, useful for foraging in trees, and of limited bipedal locomotion,
useful for carrying. Indeed, carrying seems especially promising as a cause of habitual bi-
pedalism. But there is a final potential problem: What differentiated early hominins from
ancestral chimpanzees, leading us and not them to become bipedal? Indeed, this is a critically
important question that all proposals for the origin of bipedalism must address.
In this regard it is useful to first ask whether the hominin-chimpanzee split was allopatric
or sympatric, i.e., whether the separation between the lineages was physical or behavioral.
Traditionally the East African Rift (Figure 9.2) has been cited as a physical barrier, with
chimpanzees isolated to the west and hominins to the east of the valley (e.g., Stringer &
McKie, 1996, p. 24). However, this interpretation became less plausible following the dis-
covery of “Toumai” in Chad, a location far west and north of the rift. More recent inter-
pretations tentatively suggest sympatric speciation, but don’t identify the specific behavioral
differences that might have led to the cessation of interbreeding (Elton, 2008; McBrearty &
Jablonski, 2005).
It is proposed here that a critically important factor may have been the range of en-
vironments exploited by the two lineages. Although today’s chimpanzees occupy a number
of environments (McBrearty & Jablonski, 2005), there is presumptive evidence that this was
not the case when their ancestors split from hominins. Specifically, there are no known
chimpanzee fossils older than 550,000 years. As pointed out in Chapter 2, this is probably
because most ancestral chimpanzees lived in hot, damp forest environments with acidic soils,
promoting rapid decay (Orwant, 2005).
One must always be heedful of the adage, “The absence of evidence is not evidence
of absence”. However, in this case the complete absence of ancient chimpanzee fossils in
places where hominins are (relatively) abundantly found, argues that at the split, ancestral
chimpanzees were restricted to forest environments.
To be sure, hominins also exploited forests – but they used other, more fossil-friendly
environments as well. As noted, “Toumai” exploited a diverse mosaic environment that
Bipedalism 149
Figure 9.2 East African Rift, with tectonic plate movements.

Source: ATJ map (color).jpg, CC BY-SA 3.0, Razashah1.
also included savanna, woodland, and grassland (Brunet et al., 2004; Elton, 2008). It seems
possible that this explains why hominins, and not other apes, adopted bipedalism. Hominins
needed to carry tools and weapons because a particular environment might not have appro-
priate source materials. Ancestral chimpanzees, in contrast, could depend on an unchanging
environment to provide needed materials, substantially reducing their carrying needs.
Thus, while the hominin-chimpanzee split likely involved sympatric speciation, the
greater diversity of hominin environments may have pressured toward bipedalism in a way
that did not apply to ancestral chimpanzees. Over time, behavioral differences then emerged
that created reproductive barriers between the groups. While this hypothesis of course re-
quires corroboration, it represents a potential path forward in understanding the causes of
hominin-specific bipedalism.
Consequences of bipedalism
Once bipedalism became reasonably efficient, hominins could afford to embark on hunts that
included the opportunistic collection of fruit and nuts as a secondary activity. This reversed
the quadrupedal ape practice of foraging for fruit and nuts accompanied by opportunistic
hunting. To the chimpanzee-human common ancestor, fruit was an imperative and meat a
luxury; to later hominins, meat was an imperative and fruit a luxury. The long-distance hunt
may have perfected human bipedalism (Stanford, 2003).
The achievement of habitual bipedalism was accompanied by significant changes in
anatomy. Virtually all body segments were affected, head to toe. As we have already seen, the
head moved to a more balanced position with respect to the trunk, visible in fossil skulls as a
better-centered foramen magnum that opened straight downward rather than angling slightly
backward (Figure 9.3). At the same time, the snout shortened which improved head stabi-
lization (Bramble & Lieberman, 2004).
The vertebral column and thorax

At least in australopithecines (Ward, 2002), and probably even earlier in Ardipithecus
(Lovejoy, Suwa, Spurlock, Asfaw, & White, 2009), bipedalism led to the vertebral column
becoming sinusoidally curved, allowing the trunk to be carried vertically instead of hunched
over (Figure 9.4). The shape acts as a spring (Martin, 1992). It also helps keep the body
centered over shifting feet, which has been said (perhaps a bit apocryphally) to require
“balance as fine as that required to spin a dinner plate on a broomstick” (Stanford,
2003, p. 47).
The ribcage also changed, from the inverted-cone shape of apes to a more cylinder-like
shape in modern humans (Figure 9.5). The upper narrowing in apes allows their shoulders
to more closely overhang the center of gravity, an aid to habitual arm-hanging from tree
limbs (Hunt, 1994). This narrowing was still present in Australopithecus afarensis and sediba
two to three million years ago (Schmid et al., 2013). It is often interpreted as indicating
preserved arm-hanging behavior in those species, despite their advanced bipedalism on
the ground.
However, it could simply be that the cone shape was retained until some additional factor
favored a cylinder. The Neanderthal thorax, for example, had a cone shape even though
Neanderthals were fully terrestrial (Gómez-Olivencia et al., 2018). Possibly the additional
factor favoring a cylinder was endurance running. That is more efficient with expansion of
the top of the ribcage, a widening of the shoulders, and a generalized narrowing of the thorax
(McHenry & Coffing, 2000).
Bipedalism 151
Figure 9.3 Underneath side of the gorilla and modern human skulls. The foramen magnum is posteriorly
shifted in the gorilla relative to the more central one in the human. Note that the two skulls are
not equally to scale.
Credits: Adaptation of Gorilla Male skull base.png, CC BY-SA 3.0, Didier Descouens, and Sobo 1909 41.png, public
domain, Dr. Johannes Sobotta.
The pelvis
One of the most substantial areas of change, long-recognized and carrying high significance
for childbearing, was in the pelvis. Our pelvis is lower and broader than that of a nonhuman
ape. The pelvic opening opens more distinctly downward, and the ilium (each of the bla-
delike extensions at the back of the pelvis) wraps further forward around the sides, providing
a broad attachment surface for the hugely expanded gluteus maximus (butt) muscles. These
muscles allow us to walk stably, with only one foot periodically in contact with the surface,
unlike the side-to-side rocking of apes walking bipedally. In general the shape of our pelvis is
more cup-like, cradling our internal organs (Martin, 1992; Stanford, 2003). These changes
were well advanced by the time of the australopithecines (Figure 9.6, top).
By the time of Homo erectus about a million years ago, the pelvis’ birth canal had enlarged
sufficiently to pass a baby’s head sized within the modern range (Simpson et al., 2008).
Modern humans have a pelvic opening that is more circular than that of australopithecines,
better accommodating the shape of the newborn skull (Figure 9.6, bottom; Claxton,
Hammond, Romano, Oleinik, & DeSilva, 2016; Gruss & Schmitt, 2015). However,
clearances are tighter, and compared to other mammals the pelvic bones do not spread apart
as flexibly, typically resulting in more difficult childbirth. The inflexibility may itself be an
adaptation for bipedalism, by allowing attached muscles to exert greater force (Pavlicev,
Romero, & Mitteroecker, 2020).
Figure 9.4 The modern human spinal column. C = cervical vertebrae, T = thoracic vertebrae, L = lumbar
vertebrae.
Credit: The human spinal column, CC BY 4.0, Sketchfab.
Bipedalism 153
Figure 9.5 Human versus gorilla skeleton, showing cylindrical versus cone-shaped ribcages.
Source: Primatenskelett-drawing.jpg, public domain, unknown.
The arms and hands

Also in response to bipedalism, the arms shortened, as did the fingers, which straightened.
The noticeable curvature of the fingers in Australopithecus anamensis and afarensis is a
further argument, beyond that of the ribcage’s shape, that these species remained
partially arboreal. The fingers had straightened a bit by the time of africanus (Harcourt-
Smith & Aiello, 2004; McHenry & Coffing, 2000; Ward, 2002), and continued doing
so afterward.
Figure 9.6 Pelvis in Australopithecus sediba (top) and a modern human (bottom). Note: Not to scale.
Credits: Adaptation of Pelvis MH2 Australopithecus sediba.jpg, CC BY-SA 3.0, Profberger, and Pelvis (male) 03-superior
view.png, CC BY-SA 2.1 JP, BodyParts3D.
The legs and feet

For their part the legs lengthened, allowing longer walking and running strides, and reducing
the center of gravity for a stabler stance (Bramble & Lieberman, 2004; Martin, 1992).
Reference has already been made to the longer femoral neck in early hominins, allowing the
legs to angle in so that weight was distributed more directly over the feet (Lovejoy et al.,
2002). Muscle distribution also changed, with hominins predominantly emphasizing the
quadriceps (muscles on the front of the thigh that extend it). Apes emphasize the hamstrings and
adductors (muscles on the back and inside of the thigh that move it backward and inward,
respectively).
The hominin change in emphasis improved strides by powering the forward movements
of the knee, allowing fuller extension. It also limited hip extension, which was less needed in
walking than in tree climbing (Lovejoy et al., 2002). The Achilles tendon lengthened, im-
proving the energetics of running through its spring-like storage of energy (Bramble &
Lieberman, 2004), a characteristic already present in Australopithecus afarensis 3.2 million years
ago (McNutt & DeSilva, 2020).
As the only portion of the body in direct contact with the ground, the foot changed
dramatically to promote both balance and propulsion. The major arches of the foot – one
running lengthwise and the other side-to-side (Figure 9.7) – were already prominent relative
to other apes by the time of Australopithecus afarensis, and became more so afterward. They
stiffened the foot, and allowed more efficient weight transfer while walking (Venkadesan
Bipedalism 155
Figure 9.7 The major foot arches.

Credit: Heel and Arches Closeup, CC BY 2.0, by HeelsandFeet.
et al., 2020). The hallux (big toe) also changed. In apes it is opposable and can be used to
grasp limbs when climbing. In our ancestors this function was lost, and the hallux moved into
the same plane as the other toes (Harcourt-Smith & Aiello, 2004).
Better documented is the angle of the hallux to the other toes, within that plane. In
quadupedally walking bonobos, the mean angle is about 32°, and one measured while
walking bipedally showed an angle of 28° (Vereecke, D’Août, De Clercq, Van Elsacker, &
Aerts, 2003). In the 3.66-million-year-old Laetoli footprints, believed to have been made by
Australopithecus afarensis, the hallux was at a bonobo-like 25° angle – which, as noted in
Chapter 5, is indistinguishable from that in a 5.7 million-year-old putative hominin
trackway. In marked contrast, a 4.4-million-year-old Ardipithecus ramidus specimen had the
hallux splayed away from the other toes at a whopping 68° angle, as approximated in
Figure 5.3 (Lovejoy, Latimer, Suwa, Asfaw, & White, 2009). In this, it appears to have much
more resembled gorillas than Homo sapiens (Prang, 2019).
It is interesting, and relevant to the evolution of bipedalism, that even a 25° angle could
produce dragging of the hallux, as in some prints from the Laetoli trackway (Figure 9.8). In
1.5-million-year-old fossilized footprints in Kenya, thought to have been made by Homo
ergaster or Homo erectus, the hallux was at a 14° angle (Bennett et al., 2009) and would
have been less susceptible to dragging. In Homo neanderthalensis, the angle was 11°. Now, in
Homo sapiens, it is only about 7° (Bennett et al., 2009; Pablos et al., 2019), and we certainly
do not drag our hallux.
Figure 9.8 Detail of newly uncovered prints at Laetoli. The middle print reveals a dragging hallux as the
individual stepped forward, evidenced as a trail behind the footprint.
Source: Adaptation of Southern part of the hominin trackway in test-pit L8, CC BY-SA 4.0, Fidelis T. Masao, Elgidius B.
Ichumbaki, Marco Cherin, Angelo Barili, Giovanni Boschian, Dawid A. Iurino, et al.
The substantial departure of the ramidus measurement from the bonobo and afarensis results
give strong reason to doubt that ramidus was in the direct human ancestral line. Otherwise,
the last four million years of hominin evolution has seen a smoothly progressing realignment
of the big toe, increasing its efficiency in working with the other toes to promote bipedal
locomotion.
Late anatomical developments in Homo helped improve bipedal performance when
running. These included shortened toes commencing with habilis and lengthened legs
beginning with erectus. Today, while we are relatively poor short-distance runners, we
are fairly impressive at long distances. The speeds obtainable in endurance running,
about 2.3 to 6.5 m/sec (5.1 to 14.5 miles/hr), manage to bracket the average 5.8 m/sec
(12.9 miles/hr) speed of long-distance postal horses. However, this type of running is still
metabolically more expensive, pound for pound, than it is for typical quadrupeds
(Bramble & Lieberman, 2004).
Nevertheless endurance running may tie in with long-distance hunting. Although modern
hunter-gatherers rarely engage in endurance running, it may have been an obligatory aspect
of hunting before the invention of at-a-distance weapons like spear throwers and arrows.
Endurance running allowed animals to be run down through exhaustion, permitting hunters
to approach and make a kill (Bramble & Lieberman, 2004). Even though the method in-
volves a large outlay of energy, if a large animal is killed and consumed, the ratio of energy
gains to losses exceeds 25:1 (Glaub & Hall, 2017).
Conservation and change in motor patterning

The emergence of bipedalism produced incremental change not just in anatomy but in motor
patterning. However initially, bipedalism likely conserved already existing patterns.
Bipedalism 157
D’Août and colleagues concluded that there are strong similarities in stance and gait
between quadrupedal and bipedal modes of locomotion in bonobos. The angular dis-
placement of joints is similar in the two modes, and the distribution of forces in the foot
while striding are also similar although the heel tends to make more impact during a
quadrupedal stride. The roll-off of the foot at the end of the stride shows little difference
between the two modes. The authors concluded that early bipedalism, assuming it mi-
micked these results, was likely a “free bonus” of movement patterns established with
quadrupedalism (D’Août et al., 2004).
Conservation of gait during evolution is also stressed by proponents of a less terrestrial,
more arboreal origin for bipedalism (Schmitt, 2003). Regardless of whether they are
walking quadrupedally or bipedally, primate species in general use a “compliant” gait that
absorbs shocks via flexed (bent) joints (Figure 9.9). The gait also prevents excessive vertical
movement of the center of gravity and allows long strides. That is particularly beneficial
to species walking in trees, because it minimizes branch shaking. Indeed, arboreal mar-
supials have compliant gaits similar to those of primates. Presumably a compliant style of
Figure 9.9 Flexed joints in a tripedal walk by a young chimpanzee.

Source: Adaptation of untitled, public domain, sarangib.
walking was characteristic of early hominins, and only later did the stiff, noncompliant
characteristics of modern bipedalism emerge (Larney & Larson, 2004; Schmitt, 2003).
The modern form was approximated by Australopithecus afarensis 3.4 million years ago.
Analysis of its lower limbs indicates that the heel struck first while striding with the knee
extended, which then extended further at mid-stride. This corresponds to modern, stiff
bipedalism (Ward, 2002). Others analyzing the Laetoli footprints of 3.66 million years ago
conclude that the afarensis stride was either virtually identical to that of modern humans
(Bennett, Reynolds, Morse, & Budka, 2016), or involved slightly more flexed limbs (Hatala,
Demes, & Richmond, 2016). Nevertheless all parties agree that compared to other primates,
afarensis possessed a relatively stiff and less compliant gait, one close to the modern form.
Even if it remained partially arboreal, it was well adapted to terrestrial bipedalism.
Our stiff gait’s advantage is that it conserves about 70% of expended energy from one stride
to the next, a figure nonhuman apes fall far short of achieving (Sellers et al., 2005). Thus, it
appears that a gait that minimized branch movement gave way to one that recovered energy
between successive strides.
Conclusion
All indications are that bipedalism has been a hominin feature for about as long as there have
been hominins. It was definitely present in Orrorin six million years ago, and very likely
present in “Toumai” seven million years ago. Nevertheless early hominins were simulta-
neously specialized for more than one mode of locomotion. Besides being well adapted for
bipedal walking using a remarkably modern stiff, extended stride, Australopithecus afarensis also
showed clear signs of arboreal adaptation in its cone-shaped thorax and curved fingers.
Both modes of locomotion make sense in terms of our evolutionary antecedents. The
last common ancestor of chimpanzees and humans could probably stand and take a few
steps bipedally, most often while foraging. Yet like chimpanzees, that ancestor was also
comfortable in trees. Human bipedal walking is more efficient than ape quadrupedal
walking, providing one reason for the evolution of bipedalism, but other factors must have
been at work.
The factors pushing us into habitual bipedalism have become clearer although they are not
yet a matter of consensus. Naturalistic observation of our closest relatives indicates some
capacity for bipedally carrying objects, a conclusion confirmed by experimental observations
of food carrying. A reduction in the size of the canines 6 to 7 million years ago in human
ancestors likely indicates a reduced need for them in aggressive encounters. Together these
observations suggest that carrying, including the carrying of simple weapons and other tools,
provided impetus for us to walk upright. Other possible influences include improvements in
upright foraging and in thermoregulation.
It appears that the split between hominins and chimpanzees was sympatric in that the
environments they occupied overlapped. However, the absence of chimpanzee fossils of any
significant age suggests that ancient chimpanzees were limited to hot, damp forests while
hominins exploited a mosaic of woodland, grassland, forest, and savanna. If so, hominins may
have had to carry tools and weapons to ensure that they had them in shifting environments,
providing a possible reason why humans but not chimpanzees became bipedal.
An initially compliant bipedalism yielded over three million years ago to a stiffened gait
that recovered energy from one step to the next. Then further changes beginning about two
million years ago adapted us for endurance running.
Throughout this evolutionary process, changes occurred in the hominin skeleton. The
foramen magnum became more centered in the skull, allowing the head to balance during
bipedal locomotion. The vertebral column became a curved spring. As hanging from
Bipedalism 159
branches became less common, the ribcage became more cylindrical than the cone shape
found in nonhuman apes and early hominins, and curved fingers straightened. The pelvis
became lower and broader, and its opening more circular. However, it also became less
flexible to allow greater muscle forces, resulting in more difficult childbirth.
The legs lengthened, and a longer femoral neck allowed them to angle in to distribute
weight more directly over the feet (though this was to shorten again following changes to the
pelvis). The Achilles tendon lengthened at least as early as Australopithecus afarensis 3.2 million
years ago, improving running. The feet developed prominent arches, stiffening them. The
hallux came into the same plane as the other toes, and became much less divergent over
several million years. These changes improved both balance and propulsion.
So much for our legs and feet. The next question was, what would we do with our
freed-up hands?
Section III
Perception and cognition

10 Praxis and handedness
Whether or not carrying objects led to bipedalism, bipedalism certainly had profound effects
on carrying objects. Standing upright freed the hands from any direct role in locomotion.
From that point onward they could either wither away as an unnecessary metabolic expense,
like the forelimbs of some theropod dinosaurs, or adopt new roles in the hominin lifestyle.
That they took the latter course profoundly affected the history of cognition as it relates to
the creation of objects and language.
In this chapter, we first consider the nature of praxis and its underpinnings in the brain, before
examining handedness and its primate origins and human components. The genetic foundations
of handedness are considered, as is archaeological evidence attesting to its antiquity. Finally, we
ponder why handedness exists, in both a right-handed majority and a left-handed minority.
Praxis
Consideration of how we voluntarily move, especially the hands but not limited to them,
begins with praxis – the ability to conceive, initiate, and complete movement. Although this
ability partially depends on motor pathways described earlier, brain mechanisms play a
substantial role by allowing us to conceptualize and initiate movement.
Movement-related brain areas

Several movement-related brain areas were identified by early research on the effects of brain
lesions (areas of physical damage, usually resulting from strokes or penetrating wounds).
Lesions of the primary motor cortex, the rearmost strip of the frontal lobe (see Figure 10.1),
can lead to paralysis. As we saw in Chapter 8, this strip originates the corticospinal tract that
crosses to the opposite side. The body is systematically represented within it, with the tongue
and face represented in the lowermost part, the legs and feet in the uppermost part, and the
trunk in between (see Figure 10.2). Thus, a circumscribed lesion can paralyze a single part of
the opposite side of the body. Observations like these indicate that the main function of the
primary motor cortex is to initiate movement, passing signals down the motor pathways to
produce muscular contraction.
Other brain areas, such as the premotor cortex and the supplementary motor area
(Figure 10.1) also play roles in movement. For its part the supplementary motor cortex is
activated during mental rehearsal of movement sequences. Lesions of it disrupt the voluntary
control of movement, in part (if the left hemisphere is involved) by disrupting memories of
sequential movements and their timing (Halsband & Lange, 2006).
A third area, the premotor cortex (Figure 10.1), plays a role in integrating spatial in-
formation with movement. The area activates when participants move using visual guidance,
as in reaching, writing, drawing, or in the laboratory, tracking a moving slot with a stylus.
DOI: 10.4324/9781003137863-13
164 Perception and cognition
Figure 10.1 Motor areas of the frontal lobe. The primary motor cortex is in red, the premotor cortex is in
green, and the supplementary motor area is in blue. The red and blue areas also extend onto the
medial surface of the cortex.
Source: Adaptation of Brodmann area 4 lateral.jpg, CC BY-SA 2.1 JP, BodyParts3D.
In the right hemisphere particularly, the area is involved when the integration of spatial
information is demanding, as in the early phases of motor learning using visual guidance.
Activation may switch to the left hemisphere later in learning (Halsband & Lange, 2006).
A notable aspect of the ventral portion of the premotor cortex is that it contains cells that
fire rapidly when their possessor observes the actions of others. They also fire when he or she
makes the same motions. Such mirror cells undoubtedly play a major role in skill learning
through the observation and mimicry of others (Rizzolatti, Fogassi, & Gallese, 2002). In
effect, they serve as a kind of preverbal communication system, with a teacher triggering
neural activity in the learner that aids in copying behaviors.
The parietal lobe (Figure 6.3) plays an indirect role in praxis through spatial computation
and the evaluation of sensory feedback. Although these could be viewed as perceptual, there
is increasing recognition that the parietal lobe can play a more direct role in movement.
Specifically, the intraparietal sulcus (Figure 10.3) helps direct eye movement, and in the left
hemisphere helps produce gestures. It becomes active when hand motions are targeted to
particular locations. Also, lesions in or near it interfere with reaching movements (Grefkes &
Fink, 2005; Mühlau et al., 2005).
The functions served by the premotor cortex in the frontal lobe and the intraparietal sulcus
in the parietal lobe are sufficiently similar that they are probably linked as parts of a larger
system for the control of movement. Damage to either can result in disordered gestures due
to spatial and timing errors. Although their functional differences are somewhat unclear, it
may be that the premotor area is more involved in memory aspects of movement, and the
Praxis and handedness 165
Figure 10.2 Body part representations in the primary motor cortex. The size of each part reflects the amount
of cortex devoted to it.
Source: 1421 Sensory Homunculus.jpg, CC BY 3.0, OpenStax College.
parietal area in spatial orienting and the positioning of body parts (Haaland, Harrington, &
Knight, 2000).
A final brain area involved in praxis is the cerebellum. This large structure at the rear and
base of the brain (Figure 6.3) plays a role in motor programming, specifically in “packaging”
movements as a timed sequence of components. The cerebellum also directs real-time
correction of movement due to its possession of overlaid sensory and motor maps of the
body, permitting it to detect discrepancies and issue error messages (Kolb & Whishaw, 2003).
The evolution of movement-related brain areas

Cross-species comparisons indicate that movement-related brain areas evolved at varying
times in the human ancestral line. The primary motor cortex traces at least as far back as
the origin of eutherian mammals over 160 million years ago. In contrast, interconnected
Figure 10.3 The intraparietal sulcus.

Source: Gray726 intraparietal sulcus.svg, public domain, Gray.
supplementary, premotor, and parietal motor areas date approximately from the origin of
primates 74 million years ago (Stepniewska, Preuss, & Kaas, 2006). Tree shrews, close re-
latives of primates, do not have them (Kaas, 2004a).
There have also been changes within the primate lineage. Even before the divergence of
New World from Old World monkeys about 44 million years ago, control of the forelimbs
by premotor cortex had expanded from proximal to distal musculature, and stronger con-
nections had formed between premotor cortex and surrounding brain areas. These adapta-
tions are thought to have been important to the evolution of reaching and grasping by
primate forelimbs (Stepniewska et al., 2006; Sustaita et al., 2013).
In contrast, the cerebellum is a truly ancient structure. Its first clear appearance was in
jawed fish, a group including the sharks and rays (see Figure 2.3). This places the origin of the
cerebellum about 445 million years ago. It may be even older, consisting of a few cells in
lampreys (Sugahara, Murakami, Pascual-Anaya, & Kuratani, 2017). If this homology (a simi-
larity in traits traceable to common ancestry) is accepted, the origin of the cerebellum is
pushed back to over 500 million years ago.
Evolutionary investigation of the cerebellum in primates has focused on its size relative to
the rest of the brain. An enlargement in apes relative to monkeys suggests a size shift be-
ginning about 29 million years ago. The enlargement may have been related to increases in
movement complexity and motor planning (Rilling, 2006).
The primate origins of handedness

The importance of the comparative study of handedness is that population right-handedness
(PRH) may serve as a behavioral marker for aspects of cognition that otherwise would be
difficult to uncover. More particularly, cross-species comparisons of handedness may allow
tentative conclusions regarding evolutionary changes in praxis.
Although species in which individuals show either a left or right limb preference are
common, species in which most individuals prefer the same side are less so (Stancher,
Sovrano, & Vallortigara, 2020). Population left-handedness (PLH), in which a majority favor
the left side, is sometimes reported in primates that diverged earliest from the human line. A
2005 review found that strepsirrhines tend to show PLH, an observation owing more to
lemurs than to galagos or sikafas (Papademetriou, Sheu, and Michel, 2005). However,
subsequent studies of lemurs have mostly failed to find significant population differences,
although one reported PLH (Nelson, O’Karma, Ruperti, & Novak, 2009) and another PRH
(Regaiolli, Spiezio, & Hopkins, 2016). Overall the results suggest that the primate primitive
character was either PLH, or no population tendency at all.
Modern humans, of course, show a strong PRH, a derived character. Identifying the
point of switchover to PRH is therefore of evolutionary interest. Following a massive
review of great ape handedness, involving over 1,500 individuals, Hopkins (2006) con-
cluded that in tasks taken as a whole, orangutans show no sidedness, gorillas a significantly
greater tendency than orangutans toward PRH, and the two chimpanzee species a sig-
nificant PRH. While the review found bonobos to have greater PRH than chimpanzees,
this was negated in a subsequent study (Hopkins et al., 2015).
A strengthening of PRH within primates? The roles of task and environment

These results, taken together, seem to lend themselves to the straightforward conclusion that
there has been a constant strengthening of PRH since the orangutan divergence. However,
detailed analysis shows that whether or not PRH is found in a species partially depends on the
task used to assess handedness and the environment in which it is performed. For example,
the supposedly unsided orangutans show PLH in the “tube task”. In that task, one hand holds
a tube from which food is extracted with the other, dominant hand. Orangutans also show
PLH in self-touching (Hopkins, 2006; Hopkins et al., 2011). Yet when hand use is assessed
in simple reaching or in leading locomotion, orangutans show PRH (Hopkins, 2006).
Obviously, such findings complicate any simple conclusion that orangutans show no overall
population handedness when tasks are considered as a whole. They indicate that PRH
probably has multiple components with differing evolutionary histories.
The testing environment further complicates matters. In the past, Marchant and McGrew
criticized the conclusion that chimpanzees show PRH, because the supporting evidence
came mostly from captive rather than wild animals (Marchant & McGrew, 2007). If PRH
is found only under artificial conditions, it would weaken the argument that it is a derived
character with a traceable evolutionary history prior to hominins.
Hopkins (2006) examined the nature of the testing environment in his review, and ob-
tained ambiguous results. When handedness was treated as a continuous variable, environ-
ment had no effect, suggesting that chimpanzee PRH pertains to both captive and wild apes.
However, when handedness was treated as a categorical variable, with animals classified into
one of five categories (strongly right-handed, mildly right-handed, ambiguously handed,
mildly left-handed, and strongly left-handed), environment did have an effect, with captivity
seeming to shift PRH toward a stronger form than that seen in the wild. Nevertheless, PRH
was found in both captive and wild animals. Most recently, a study of wild-born orphan
bonobos in an African sanctuary tends to confirm the existence of PRH (Neufuss, Humle,
Cremaschi, & Kivell, 2017), indicating that it is not just an artifact of close captivity.
That conclusion is fortunate, because a critically important piece of the PRH puzzle comes
from a captive chimpanzee study (Wesley et al., 2002). Each of 100 chimpanzees were given
six tasks multiple times, allowing their handedness to be assessed for each task. The results
were then subjected to a statistical technique known as factor analysis, allowing relationships
among the tasks to be determined. For example, if individuals who show right-handedness
for one task also show it for a second task, while those who show left-handedness for one also
show it for the other, the two tasks are related. Factor analysis will assign them to the same
group of measures (i.e., the same factor).
Wesley et al. identified two factors in their study. One consisted of the handedness tasks of
reaching (picking up food while in a tripedal posture), gesturing (using one hand in a
communication gesture), biased feeding (manipulating food placed systematically into the left
or right hand), and to a lesser extent, feeding (using one hand to bring food to the mouth
while holding other food with the other hand). A second factor consisted of the tube task in
its original form, and a modified version in which only one end of the tube was inserted into
and affixed to the animal’s cage.
Because two different factors were found, they represent two separate components
of handedness, with one involving reaching, gesturing, and feeding, and the other in-
volving tube task handedness. Confirmation that these are two separate factors came from
a later developmental study, reporting that reaching handedness in young chimpanzees
predicted gesturing handedness a decade later, while tube task handedness did not
(Hopkins et al., 2005).
Components of primate handedness

The significance of the factor analytic results is that they indicate the existence of at least two
different components of ape handedness with potentially different evolutionary histories.
Examining the components might help account for some of the reported handedness dif-
ferences between species.
Accordingly it is important to consider individual tasks, in the expectation that their
results may differ from those based on tasks as a group. Considering reaching first – partially
comprising one of the factors in Wesley et al. (2002) – both orangutans and bonobos (and in
strong trends, common chimpanzees and gorillas) have shown PRH (Hopkins, 2006).
Similarly, in studies of chimpanzees and gorillas by Prieur and colleagues, gestures – likewise
part of the factor – have shown striking PRH (Prieur, Pika, Barbu, & Blois-Heulin, 2016a,
2016b). Altogether, then, the reaching and gesture component of handedness seems likely to
have shown PRH from before the divergence of orangutans, not afterward as suggested by
tasks-as-a-group analysis.
In contrast, in the tube task – the other factor in Wesley et al. – orangutans have shown
PLH (Hopkins, 2006; Meguerditchian et al., 2015). So have the earlier-diverging lesser apes
(Morino, Uchikoshi, Bercovitch, & Hopkins, 2017). Lesser apes have also shown PLH when
collecting and drinking water from holes in tree trunks (Morino, 2011), a behavior somewhat
paralleling the tube task. Chimpanzees, however, have shown PRH in the tube task, as have
gorillas to a seemingly similar though nonsignificant degree (possibly due to a much smaller
sample size; Hopkins, 2006). Thus, the tube task component of handedness seems to have
shifted from PLH to PRH sometime after the orangutan divergence.
Putting these considerations together implicates at least two independent handedness
developments in the pre-hominin ancestral line. PRH in the kind of motor activity involved
in reaching, gesturing, and feeding is an older character predating the orangutan divergence
15 million years ago. How long it predated that divergence, however, is unclear. Although
communication gestures in baboons and Tonkean macaques, both Old World monkeys,
likewise show PRH (Meunier, Fizet, & Vauclair, 2013), reaching in golden snub-nosed
monkeys, another Old World species, shows PLH (Fu et al., 2019). These findings suggest
that the core of the reaching-gesturing-feeding component of PRH extends back sometime
before 15 million years ago, but possibly not as far as the Old World monkey divergence
29 million years ago. Given the nature of the underlying tasks, this component is perhaps best
characterized as unskilled handedness.
In contrast PRH in the kind of motor activity involved in the tube task apparently
postdates the orangutan divergence. However, it probably predates the gorilla divergence,
not only because gorillas show a strong tendency toward PRH on the tube task but also
because gorillas are significantly right-handed in the similar task of bimanual feeding. There,
one hand (usually the left) provides grip, and the other hand (usually the right) performs
delicate food preparation actions (Hopkins, 2006; Tabiow & Forrester, 2013). This seems
conceptually similar to the tube task. The cooperative bimanual praxis that both involve
seems more highly skilled than reaching-gesturing-feeding, and so this component is perhaps
best characterized as skilled handedness.
However, it is important to note that there is evidence of a third component of
chimpanzee handedness not captured by the factor analytic study of Wesley et al. Termite
fishing is a behavior observed in wild chimpanzees, in which a twig is prepared and then
inserted into termite mounds. Termites defensively latch on to the twig, and are then
pulled out of the mound with it and are eaten. Combining small samples of observations
collected in the wild, Hopkins (2006) found a significant PLH, not PRH, for this
behavior. However in the largest termite-fishing study to date, there was no significant
difference between hands (Sanz, Morgan, & Hopkins, 2016).
Altogether then, termite fishing shows either PLH or no hand difference. Because it is not
in accord with the more general PRH that is observed, it presumably represents a third
component of chimpanzee handedness. Notably, termite fishing involves tool insertion. It
also differs not only from reaching-gesturing-feeding but also from the tube task in that tools,
not fingers, perform the required action. This could emphasize spatial perception more than
other handedness behaviors and lead to the participation of right hemisphere/left hand
control mechanisms. The importance of this third component of handedness will soon be-
come apparent, when distinctions among unskilled, skilled, and insertion handedness are
shown to be relevant to human handedness as well.
Components of human handedness

Human PRH is much more pronounced than that of other primates. Whereas right-
handedness is characteristic of about 60% of chimpanzees as assessed in a broad variety
of tasks (Hopkins, 2006), it characterizes somewhat over 90% of humans (Cochet &
Byrne, 2013; Prieur, Barbu, & Blois-Heulin, 2018). The percentage of human right-
handedness is about the same, whether it is assessed through actual task performance, or
by questionnaire as more commonly practiced. PRH is universal in all human populations
that have been studied, although there is some variation in incidence. Thus, as assessed
by throwing, the incidence of left-handedness in Papua New Guinea is over twice
that in the United States, with the United Kingdom falling between these extremes
(Raymond & Pontier, 2004).
Extrapolating from primate observations, it seems reasonable to expect at least three
independent components to human handedness: An unskilled component, a skilled
component, and a component involving insertion. This has been confirmed. One of the
largest factor analytic studies of handedness, both in terms of participants (1,275) and the
number of assessed handedness behaviors (47), was conducted in Japan and Canada by Ida
and Bryden (1996). Questionnaire data were subjected to factor analysis, and three factors
were extracted. One involved unskilled handedness, and was comprised of 16 items in-
cluding waving, pointing, and picking up small objects. Another factor reflected skilled
handedness, and was comprised of 19 items including writing, drawing, hammering,
throwing, using a toothbrush, and striking a match. Finally, the third factor involved
handedness as assessed by insertion and turning movements. This factor involved 12 items
including inserting a key, pulling a key, turning a key, and shuffling cards (which, it should
be noted, is an insertion task). The first two factors substantially replicated those of an
earlier study involving fewer participants and fewer handedness items. Although the earlier
study did not use any of the turning-insertion-card playing items of the later one, it is
intriguing that an item involving winding a stop watch, which involves a turning motion,
itself defined a separate factor, apparently prefiguring the emergence of that factor in the
later study (Steenhuis & Bryden, 1989).
Thus, the same three handedness components found in chimpanzees (skilled, unskilled,
and insertion handedness) return strong echoes in human data. This is in spite of the much
higher incidence of generalized right-handedness in humans than in chimpanzees.
Clearly, an important question to ask about human PRH is whether it can be attributed
to a simple strengthening of the components present in chimpanzees. Some strengthening
has certainly occurred, as is evident in the data of Ida and Bryden (1996) and others. For
the skilled component, 94% of their participants were right-handed using a forced-choice
definition of handedness (i.e., splitting those with ambiguous handedness into left- or
right-handers). This figure contrasts markedly with the 57% figure found for the skilled
tube task in chimpanzees (Hopkins, 2006). Similarly for the turning-insertion component,
89% of humans were right-handed, compared to between 37% and 54% for chimpanzee
termite fishing (Lonsdorf & Hopkins, 2005; Sanz et al., 2016). Thus, it is clear that
strengthening occurred in these two components of handedness, accompanied by a pos-
sible reversal in the turning-insertion component from PLH to PRH. Perhaps an initial
involvement of the right hemisphere of the brain in insertion tasks, because of their spatial
component, has in us given way to predominant left hemisphere involvement due to
motor programming.
Against this background, a strikingly different result was found for the remaining com-
ponent. For unskilled handedness, 58% of humans were right-handed (Ida & Bryden, 1996).
This differs negligibly from the 54% value for chimpanzee reaching, among those individuals
showing significant handedness in reaching. It also differs minimally from the 60% value
found in all apes for reaching, gesturing, and feeding taken collectively, although ape ges-
turing taken alone shows markedly more right-handedness (Prieur, Pika, Barbu, & Blois-
Heulin, 2016a, 2016b; Hopkins, 2006).
By the criterion of percent incidence, then, the phylogenetically oldest (unskilled)
handedness component appears the least changed in humans, while two newer components
related to skilled, precise hand use have undergone the greatest change. Changes in PRH
thus seem to parallel increased human capabilities in praxis. Table 10.1 summarizes some of
the differences between handedness components.
Table 10.1 Three components of PRH, as defined by factor analysis, with inferred hominin trends
since the last chimpanzee-human common ancestor. aft = after, bef = before, diff = difference,
mya = million years ago
Component Appearance Examples Hominin trend
unskilled bef 15 mya reaching, gesturing, pointing unchanged PRH

skilled ~12 mya tube task, writing, hammering PRH → greater PRH
insertion-turning aft 7.5 mya termite fishing, key insertion PLH or no diff → PRH
Genetic foundations
Tracing the evolutionary background of handedness implicitly assumes that it is under
genetic influence. Otherwise it would not be subject to natural selection. But is this a
reasonable assumption? In this section, we consider evidence for a genetic foundation of
handedness.
Family resemblances
If handedness is under at least some genetic control, there should be resemblances between
family members. Chimpanzee studies generally support this. Thus, in wild chimpanzees using
tools, or performing the tube task, an individual’s handedness is moderately related to that of
its mother (Hopkins, 2006; Hopkins, Wesley, Russell, & Schapiro, 2006). Sibling resem-
blances pertain as well: For handedness assessed by throwing hand, siblings show concordant
(same-sided) handedness to an extent greater than chance (Hopkins, Russell, Cantalupo,
Freeman, & Schapiro, 2005).
These results are certainly consistent with a genetic influence on handedness. Caution
should be observed, however, because they may also be consistent with nongenetic
factors, i.e., mothers or siblings may introduce environmental pressures toward similar
handedness.
In human handedness research, twin studies have a long history, with the first handedness
comparison of monozygotic (identical) and dizygotic (nonidentical or fraternal) twins dating
back to research by Siemens in 1924 (Medland, Duffy, Wright, Geffen, and Martin, 2006).
Greater concordance in handedness between monozygotic twins is reported, an outcome
consistent with a genetic influence although interpretation is clouded by greater similarity in
the prenatal and postnatal environments of such twins. Medland et al. (2006) reviewed 34
studies, beginning with Siemens’ work, and concluded that about 25% of variation in
handedness can be attributed to genetic factors – or in other words, that handedness is 25%
heritable. The remaining 75% is due to unknown environmental factors.
Thus, the scientific literature examining family resemblances is certainly consistent with a
genetic influence on handedness, although it cannot be regarded as completely conclusive.
Genetic models
Several specific genetic models of handedness have been proposed. The most influential is
the right shift theory of Marian Annett, a version of which was first proposed in the 1970s.
This states that human handedness is the product of a bell-shaped distribution in com-
bination with a right-shift allele that is present in some individuals and not others. By
itself, the bell-shaped distribution would lead to equal numbers of left- and right-handers,
as well as a large proportion of persons with mixed handedness. However, according to
the model the distribution is shifted rightward in those with the allele, resulting in a
predominance of right-handedness. Furthermore, depending on the task, the sub-
population of individuals with two copies of the allele, one on each of a pair of chro-
mosomes, may be shifted more strongly rightward than those with only one copy
(Annett, 1998). More recently, Annett addressed the issue of how the model might
account for the reduced PRH in chimpanzees, reporting a right-shift factor similar to that
in humans but reduced in strength (Annett, 2006).
The right shift theory makes no distinction between genders, and so the involved gene is
presumed to be an autosomal one – i.e., a gene located elsewhere than on the sex-determining
X and Y chromosomes. McManus and Bryden (1992), however, proposed that in addition
there is a recessive modifier gene located on the X chromosome that can suppress the effect
of the autosomal gene. Such a gene, they argued, could account for the existence of a
“maternal effect” in which left-handed mothers tend to produce more left-handed offspring
than do left-handed fathers (McKeever, 2000; McManus & Bryden, 1992).
A problem with both the autosomal and X-chromosome right shift theories is that testing
them largely depends on fitting handedness frequency data to the models. While the fits can
be quite good, such data could be viewed as insufficiently weighty to establish the models’
validity. This is particularly the case when different studies produce different frequencies. For
example, McKeever (2000) reported data showing that in families with one left- and one
right-handed parent, left-handed mothers produced left-handed sons (a) more frequently
than did left-handed fathers, and (b) more frequently than they did left-handed daughters.
Both observations are consistent with a handedness-related gene on the X chromosome, but
as McKeever pointed out, earlier studies failed to produce similar findings.
Individual genes
Other evidence emerges from studies relating specific genes to handedness. Laval et al.,
(1998) measured handedness by the speed of movement of pegs across a pegboard, and found
an allele on the X chromosome to be associated with left-handedness. However, the result is
not as supportive of the McManus and Bryden version of right shift theory, as initially
appears, because right shift theory states that there is no genetic left-handedness, only genetic
right-handedness.
A second discovery was that a pegboard measure of handedness correlated to the presence
of a specific gene on chromosome 2 (Francks et al., 2003), since designated LRRTM1. So
far, though, the relationship has been found only in clinical, and not nonclinical populations
(Beste et al., 2018). Also, the gene acts in a manner quite unlike that predicted by the right
shift theories, with greater father-to-child than mother-to-child genetic similarity across
multiple samples.
A third gene affecting handedness appears to be located on chromosome 12. It is related to
writing and drawing – i.e., the skilled component of handedness (Warren, Stern, Duggirala,
Dyer, & Almasy, 2006). That is one of the autosomal chromosomes, which might favor
Annett’s right shift theory. However, it remains to be seen whether a specific genetic locus
can be identified and if so, whether the gene works in right-shift fashion.
Additionally, an allele of a gene on chromosome 15, designated PCSK6, has been found to
be correlated to handedness as measured by a pegboard task. In an individual, each copy of
the allele shifts handedness rightward a small amount. Yet so far, the correlation has only been
found in reading disabled individuals, not in normal readers (Brandler et al., 2013).
Finally, Wiberg and colleagues have examined linkages between genes and handedness in
what is by far the largest sample to date, about 38,000 left-handers and nearly 360,000 right-
handers. Four genes were identified, but none were the same ones identified in the other
studies. Although one was on chromosome 2 like the LRRTM1 gene of Francks et al.
(2003), it was a different gene designated MAP2, at a different location. The other three
genes were on chromosomes not previously implicated in handedness – chromosomes 6, 17,
and 22 (Wiberg et al., 2019).
It should be noted that if there are several genes influencing handedness, all operating in
different fashion, it is unlikely that a simple genetic model of handedness will be found to
apply. In that regard some studies of either the entire genome or exome (the reduced portion
of the genome that codes for proteins) have failed to identify any genes with a major in-
fluence on handedness (Armour, Davison, & McManus, 2014; Kavaklioglu, Ajmal, Hameed,
& Francks, 2016).
What accounts for the weakness of single-gene effects on handedness? It appears to be an
instance of what had been called the missing heritability problem – the observation that even
when single gene effects are cumulated, they usually don’t account for the full heritability of a
behavior or characteristic (Bourrat & Lu, 2017). Even in the massive whole-genome study of
Wiberg et al. (2019), the four identified genes together only accounted for about 1% of the
variability in handedness – comparing unfavorably to the 25% heritability deduced from twin
studies. Thus, one reason for “missing heritability” is that each relevant gene often has only a
tiny effect on the characteristic. If so, then it can only be hoped that after a sufficient number
of massive studies have been conducted, a fuller picture will emerge. But more funda-
mentally, the problem may trace to the interactivity of genetic effects: The impact of a gene
may depend on the status of other genes, on the environment, or on the carrier’s stage of
development. All can lead to underestimating the size of genetic effects.
Nevertheless, indirect evidence from family resemblances as well as direct evidence from
studies of specific genes does support the existence of genetic influences on human hand-
edness. These discoveries lend weight to the outcome of comparative analysis indicating that
human handedness is an elaboration of earlier forms of primate handedness, and has been
subject to evolutionary forces.
Archaeological evidence
Having considered the evolution and genetics of handedness, and more specifically, of PRH,
a logical next question is to ask how far back hominins showed evidence of it. As it happens,
there is a rich and continuous record of PRH dating back nearly two million years.
The fossils of two hominins from 1.5 to 1.8 million years ago both suggest the presence of
right-handedness, though in different ways. An analysis of teeth from a specimen attributed
to Homo habilis, dating from 1.8 million years ago, indicates an increased number of scratches
on the individual’s right. Presumably the scratches resulted from holding material in the teeth
while cutting with a stone tool held by one hand, usually the right, resulting in occasional
accidental contact with the teeth (Frayer et al., 2016). In the other case, a 1.5-million-year
old Homo erectus individual, it was a larger deltoid (shoulder) muscle attachment groove on
the right clavicle that led to an assessment of right-handedness (Cashmore, Uomini, &
Chapelain, 2008). While only two cases are not conclusive evidence of PRH within their
time period, they are suggestive.
The oldest artifactual evidence of PRH in humans derives from the flakes and cores of stone
tools. When modern tool knappers work stone, they tend to hold the core (the stone from
which the tool is made) in the left hand, striking flakes (stone fragments) from it using a
striking stone held in the right hand. This distribution of effort undoubtedly traces to the
greater skill and precision of the right hand of most people.
The largely left-right distribution of core and striking stone has consequences for the
flakes struck from the core. Examination shows that the flakes have a characteristic form
involving the striking platform (the small flat surface where the blow landed). According to
Toth (1985), as the core is rotated clockwise for repeated striking, the striking platform of
a flake struck off by the right hand has a scar to the left and a weathered outer surface to
the right, when oriented upward. A left-handed knapper would presumably show the
opposite orientation of flakes, resulting from holding the core in the right hand, striking
flakes off with the left, and rotating the core counter-clockwise. Thus, collecting flakes,
and analyzing the location of the scar relative to the striking platform, may allow an
inference about the handedness of the knapper.
Modern-day counts of flakes produced by right-handed knappers show that the numerical
difference between “left-handed” and “right-handed” flakes is not large, perhaps because
these tendencies are inherently small in size, but perhaps also because a fatiguing knapper may
strike differently or even change hands from time to time. Nicholas Toth, an experienced
right-handed knapper, counted his own directional flakes and found that 56% of them were
right-handed while 44% were left-handed (Toth, 1985). Similarly, Pobiner (1999) reported
that seven right-handed students produced right-left flakes in a 60%-40% split. Less strikingly
(no pun intended), Bargalló and Mosquera (2014) reported knapping results from eight right-
handed and seven left-handed university students in Spain, which can be characterized as a
51%-49% right-left split for right handers and a 50%-50% split for left-handers. However, the
Spanish splits are based on median values across participants, which may minimize differences
compared to the overall frequency counts used by Toth and Pobiner.
The relevance, of course, is that the same analysis can be applied to archaeological col-
lections of flakes. The oldest that have been analyzed were discovered at Koobi Fora, Kenya,
and date to 1.5 million years ago. When classified, 57% were found to be right-handed
(Toth, 1985), a significant deviation from 50% given the sample size. The figure is not
significantly deviant from the 60% proportion produced by the modern right-handed
knappers of Pobiner. The Koobi Fora knappers therefore appear to have been predominantly
right-handed.
The second oldest sample is from Ambrona, Spain, dating to about 350,000 years ago,
where 61% of the flakes were right-handed (Toth, 1985), again significantly divergent from a
50% value. A sample of Neanderthal flakes, dating to about 180,000 years ago, also showed
PRH (Cornford, 1986). While an archaeological sample of flakes produced by Australian
aborigines, of uncertain age but less than 50,000 years old, showed a right-handed percentage
of only 51% (Pobiner, 1999), that did not differ significantly from the modern 60% value.
Thus, the simplest interpretation of the combined results is that humans have shown con-
sistent PRH from the time of the oldest stone tools that have been assessed, dating from 1.5
million years ago.
Nevertheless, some caution should be observed before accepting these results. Uomini
(2006) argued for the rejection of Toth’s methodology, in part because she observed no
consistency across modern knappers in the direction of rotation of the core. It is not clear,
however, how the repeated observations of asymmetry in archaeological assemblies of flakes
are otherwise to be explained, except by predominant right-handedness.
Uomini did accept as valid another study of asymmetry in lithic assemblages, that of
Phillipson (1997). After analyzing modifications to the edges of 54 handaxes from Kenya,
dated at about one million years old, Phillipson concluded that 51 were probably intended to
be used by one hand or the other. Of those, 45 (88%) were intended for right-handers, and
11 (12%) for left-handers. Note that besides enjoying a potentially better-grounded meth-
odology than that of Toth, this approach has the additional advantage of specifying specific
handedness percentages rather than a general population tendency.
As already indicated, teeth can also indicate handedness through asymmetric scratching,
pitting, and chipping by tools. You can simulate this by using your dominant hand to place a
pen cap between your teeth, and carefully guiding the pen into it. Then imagine that you
missed with an edged stone!
A sample of damaged teeth from Homo heidelbergensis in Spain, dating to before 530,000
years ago, revealed that all 20 individuals were right-handed (Lozano, Mosquera, de Castro,
Arsuaga, & Carbonell, 2009). Neanderthals, too, show handedness with this methodology,
with 29 of 31 individuals (94%) right-handed across two samples (Fox and Frayer, 1997;
Estalrrich & Rosas, 2013). It therefore seems that both Homo heidelbergensis and Homo
neanderthalensis showed strong PRH.
Tools also figured in an assessment of handedness by Semenov (1970), reporting that stone
scrapers from upper Paleolithic sites (10,000–40,000 years ago) showed traces of greater wear
on the right side, indicating right-handed use. Some 80% of scrapers were classified as right-
handed, a trend claimed to be visible even in published depictions.
Cave art supports the existence of PRH in Homo sapiens 10,000–30,000 years ago in the
form of negative hands, each of which is the outline of a hand held against the rock and painted
by blowing pigment through a tube held by the other, usually dominant hand. Of 507
known negative hands from caves in France and Spain, 77% are outlines of the left hand,
implying PRH. Confirming this, the identical 77% figure has been observed in a large sample
of university students producing negative hands with a similar technique (who, of course,
would be expected to be about 90% right-handed). Furthermore, in these modern would-be
troglodytes, throwing and writing handedness was correlated with which hand held the tube
(Faurie & Raymond, 2004).
Finally, a study of artistic representation of hand usage over the past 5000 years reveals a
stable PRH over that period. Instances of one-handed use of a tool or weapon were tallied on
the assumption that models held these artifacts in their preferred hands. Across the years, with
only minor and seemingly random variation, 93% were right-handed (Coren & Porac, 1977).
In summary, the archaeological evidence pertaining to human handedness is consistent:
PRH has existed over at least the past 1.5 to 1.8 million years, probably on the order of 90%
of individuals. In their general direction these conclusions conform to expectations from the
observed PRH in apes, and they suggest that the quantitative shift from the approximately
60% PRH found in apes to 90% in humans, dates back at least to the beginning of the genus
Homo. It may date even further back, as archaeology is silent on the matter before 1.8 million
years ago.
Why handedness?
Perhaps the most important question about handedness, specifically PRH, is why it exists at
all. The answer is likely to imply something important about the evolution of human
cognition as expressed through hand movement.
It is proposed here that PRH reflects the evolution of mechanisms of praxis that brought
the timing and sequencing of movement under control of the left hemisphere of the brain
(Leinen, Panzer, & Shea, 2016; Serrian & Sovijärvi-Spapé, 2015). Having begun as a simple
mechanism underlying the relatively gross movements of reaching, gesturing, and pointing, it
became progressively differentiated into a more skilled component supporting precision
movement about 12 million years ago, and then sometime after 7.5 million years ago, one
showing sidedness in the complex insertion and turning manipulations of tools. Throughout
this evolutionary history, operation of left hemisphere mechanisms of praxis presumably
drove a preferential use of the right hand simply because of the predominance of contralateral
motor connections. The advantage was a system that operated more smoothly and with less
delay than one requiring cross-hemisphere coordination.
At present it is difficult to reach definite conclusions about the evolution of brain changes
that supported increasing manual skill in general and PRH in particular. However, three
brain areas have been identified that will very likely prove relevant in future research.
First, monkey and human unskilled movements have in common an activation of primary
motor cortex opposite the hand (Rizzolatti et al., 2002). It may be, therefore, that the basis of
the most primitive form of PRH is asymmetry in the hand area of the primary motor cortex.
This asymmetric anatomy appears to exert influence even over skilled handedness, although
that likely involves other anatomical regions as well. Thus, in chimpanzees, not only reaching
and feeding but also tube task handedness, all appear to be related to asymmetry in the
volume of the hand area of the primary motor cortex (Dadda, Cantalupo, & Hopkins, 2006;
Taglialatela, Cantalupo, & Hopkins, 2006).
Figure 10.4 Brodmann areas of the human brain. Lobes: F = frontal, P = parietal, T = temporal, O =
occipital.
Source: Brodmann areas and lobes of the left hemisphere, licensed from Elsevier under STM Permissions Guidelines.
A second highly relevant brain area is a portion of the ventral premotor area in Old World
monkeys known as F5. This area appears to be anatomically homologous to human
Brodmann area 44 (Figure 10.4), located in the inferior frontal gyrus (Rizzolatti et al., 2002).
While area 44 exists on both sides of the brain, in the left hemisphere it is part of Broca’s area
and plays a major role in the production of speech. Notably, gesture, hammering, and termite
fishing handedness – representing all three of the handedness components in Table 10.1 – are
related to asymmetry in the chimpanzee inferior frontal gyrus, with it tending to be larger on
the left (Hopkins, Russell, & Cantalupo, 2007; Taglialatela et al., 2006).
F5 is of note because it is the location of mirror cells, which in the monkey are active
during the production of specific actions such as grasping, holding, and tearing. They are also
active when the same actions are observed in others. In humans area 44 becomes active
not only during speech production, but also when manipulating objects and especially when
executing precision grips, as we often do when using tools. Simply observing tool use, or
even tools themselves, also results in area 44 activation (Rizzolatti et al., 2002). Thus, it
appears to be one location of mirror cells in humans, with neighboring area 6 likely re-
presenting another (Cerri et al., 2015; Cook, Bird, Catmure, Press, & Heyes, 2014; de la
Rosa, Schillinger, Bülthoff, Schulz, & Uludag, 2016).
Significantly, in chimpanzees, use of a precision index finger-thumb grip is more fre-
quently performed by the right hand than by the left (Hopkins et al., 2005). This seems
similar to human right-handedness in object manipulation and tool use. Therefore it may be
that the evolution of asymmetry in area F5/44, favoring the left hemisphere, is what sup-
ported the fuller emergence of the more skilled form of PRH that is observed in primate
communicative gestures, and that in humans supports the use of simple tools. As indicated
above, comparative analysis suggests this development occurred about 12 million years ago.
However, the area itself is obviously older than its asymmetry. Macaques have an area
F5/44 (Petrides & Pandya, 2009), suggesting that it emerged no later than the time of
the Old World monkey divergence 29 million years ago. That put a critical anatomical
substrate into place long before the development of skilled handedness. Its seeds may date
back even further than that, because mirror neurons have been found in the marmoset
homolog of area F5 (Suzuki et al., 2015), and the New World monkey divergence was
44 million years ago.
A final brain area that has been implicated in primate handedness is the “pli-de-passage
fronto-parietal moyen parietale” (PPFM). This is a gyrus buried along the central sulcus,
connecting the precentral and postcentral gyri; i.e., under the dark line between
Brodmann areas 4 and 1–2-3 in Figure 10.4. In chimpanzees, differences in speed of
performance of a simulated termite fishing task correlate to anatomical asymmetry of the
PPFM, such that individuals who are faster with the right hand show a larger PPFM as well
as a larger inferior frontal gyrus in the left hemisphere. Individuals faster with the left hand
show the opposite, a larger PPFM and inferior frontal gyrus in the right hemisphere
(Hopkins et al., 2017). Unfortunately it is not yet known whether this result is specific to
the insertion-turning component of handedness, or generalizes to the unskilled and skilled
components as well.
While asymmetries of the primary motor cortex, F5, and PPFM are correlated to primate
handedness, it is not yet clear how they can account for mutual independence of the three
components of handedness (unskilled, skilled, and insertion-turning). That is an issue that
must remain to future research.
Why left-handedness?
In spite of the overwhelming right-handedness of human populations, nearly 10% of people
remain left-handed. That has probably been the case for well over a million years. What
accounts for the maintenance of this minority?
One popular view is that creativity is more often associated with left-handedness than
right-handedness. Could it be that a “creative edge” is what maintains left-handers in the
population? Some studies report increased percentages of left-handers in music or the visual
arts, or higher scores on tests of creativity or divergent thinking in left-handers relative to
right-handers. However, a literature review shows that on balance, there is no evidence for
increased creative excellence in left-handers in music, the visual arts, or literature (Heilman,
2005). It therefore seems unlikely that the maintenance of left-handedness can be accounted
for by increased creativity, if there has been no increased production of creative products by
left-handers.
In contrast, one hypothesis receiving empirical support is that in violent societies, left-
handers enjoy a survival advantage because of their unorthodox style in confrontational
fighting. The offensive and defensive hands, which in most right-handers are the right and
left respectively, are more often left and right in left-handers. Unfamiliarity with this reversal
puts right-handers at a disadvantage compared to their left-handed opponents, who are more
likely to have seen instances of their adversaries’ opposite style. Consistent with the un-
orthodox style hypothesis, sizeable increases in the incidence of left-handers are observed in
interactive sports like martial arts, table tennis, and ice hockey, relative to noninteractive
sports like swimming, skiing, and archery (Raymond, Pontier, Dufour, & Møller, 1996;
Richardson & Gilman, 2019).
The analysis of homicide rates and the incidence of left-handedness in eight traditional
societies has lent further support to the hypothesis by finding a strong correlation between
the two, as shown in Figure 10.5 (Faurie & Raymond, 2005). Left-handedness increases as
homicide rates increase, as predicted by the hypothesis that left-handers have an advantage in
confrontational conflict.
By any reasonable interpretation of the daily news, even in developed societies old-
fashioned arms-length murder remains a popular means of dispensing with adversaries.
Of the 63,661 murders committed in the United States in 2011–2015, 23% were by way of
Figure 10.5 The correlation (r = +.83) between homicide and left-handedness, across eight traditional
societies.
knives, blunt objects, beatings, drownings, stranglings, or asphyxiations – and that does not
even include the 48% committed with handguns, many of which were surely arms-length
confrontations (FBI, 2018). Thus, it seems possible that confrontational conflict continues to
play a role in maintaining left-handedness even in modern western society.
Presumably the strength of this effect has outweighed any disadvantage that left-handers
suffer in having motor timing and sequencing represented in the left hemisphere of the brain,
but control of the preferred hand in the right hemisphere. As discussed earlier, this should
result in a need for cross-hemisphere coordination, resulting in a system that works less
smoothly and with more delay.
Conclusion
The view developed in this chapter is that handedness has multiple components whose causes
ultimately trace to the same roots, namely a preponderance of left hemisphere involvement in
praxis. Taking an anatomical point of view, lesions to the primary cortex in the left hemi-
sphere can cause a paralysis of the right hand. Damage to the supplementary motor cortex,
particularly in the left hemisphere, can lead to disruption of movement rhythms. Although
the premotor cortex of the right hemisphere integrates spatial cues into movement, later in
movement learning left hemisphere influence predominates. Notably, the ventral portion of
premotor cortex is one important site of mirror cells that respond to observation of the
actions of others, and that fire when the observer makes the same motions. The parietal
lobe plays an indirect role in movement through spatial computation and sensory feedback
evaluation, but also a more direct role, with the intraparietal sulcus integrating spatial cues
with motion control. Finally, the cerebellum corrects movement errors.
The aforementioned areas emerged over many millions of years of evolution in the human
ancestral line. Comparative approaches suggest the beginnings of the cerebellum date back at
least 445 million years. Primary motor cortex dates from over 160 million years ago, and
interconnections between supplementary, premotor, and parietal motor areas date from
74 million years ago. By 44 million years ago the premotor cortex exerted control over distal
musculature. Finally, enlargement of the cerebellum relative to the rest of the brain likely
started about 29 million years ago.
A striking aspect of human praxis is the existence of population right-handedness (PRH),
with about a 90% incidence. Its roots extend at least 15 million years ago, and possibly
further. PRH likely began with a simple anatomical imbalance, perhaps in the hand area of
the primary motor cortex, that produced a slight handedness effect in reaching, gesturing,
and feeding.
Later developments, it is proposed, built upon the initial imbalance, exploiting areas
increasingly working in tandem with primary cortex. At some point in the human-ape
line, subsequent to the divergence of orangutans 15 million years ago but prior to that of
gorillas nine million years ago, a more skilled component of praxis emerged in the left
hemisphere. It likely exploited a neurological substrate, namely ventral premotor cortex, in
the production of communication gestures as well as in tool-related learning and ma-
nipulation. Further developments in manual praxis involved the kinds of spatial manip-
ulations involved in insertion and turning motions. Their control may have started in the
right hemisphere in the common ancestor of humans and chimpanzees prior to 7.5 million
years ago, but transferred to the left in humans as part of the motor programming functions
of the human left hemisphere.
Investigations of genetic influences on human handedness have a long history, but have
most recently focused on specific genes. So far, it appears that genetic determination of
handedness is controlled by a number of genes, each having a very small impact. Such studies
lend weight to the susceptibility of handedness to evolutionary influences even though we
are far from identifying the full set of genes that make it 25% heritable.
Archaeological evidence, while sometimes controversial, consistently shows hominin
PRH as far back as inferences can be made, about 1.5 to 1.8 million years ago. It consists of
lateralized tooth scratches, asymmetric muscle attachments to bone, directional flaking of
stone tools, and depictions of hands in caves and historical art.
PRH probably exists because praxis mechanisms evolved to bring the timing and se-
quencing of movement under control of the left hemisphere, eliminating the need for their
cross-hemisphere coordination. Both monkey and human simple reaching involves the
activation of primary motor cortex opposite the hand, and in chimpanzees, reaching and
feeding handedness is related to primary cortex asymmetry. Premotor cortex plays a critical
role, with all components of PRH in chimpanzees proving to be related to inferior frontal
gyrus asymmetry. Notably, the gyrus is also a site of mirror neurons.
Left-handedness, however, has been consistently maintained at roughly 10% of the human
population, begging the question of what advantage it confers. The preliminary view that it
affords a “creative edge” appears not to be true. Its maintenance may depend instead on the
existence of confrontational fighting. By using an unfamiliar, unorthodox style, left-handers
enjoy an advantage over right-handers. Thus, the higher the level of homicide in traditional
societies, the higher the incidence of left-handedness. Left-handers also tend to predominate
in confrontational sports like martial arts and ice hockey.
11 Tools and planning
Tools were once considered uniquely human artifacts. However, scientists have known
since 1917 that chimpanzees both use and manufacture tools. In that year Wolfgang
Köhler reported that captive chimpanzees at Tenerife in the Canary Islands used sticks to
retrieve food. They sometimes inserted a thinner tube inside a thicker one to extend their
reach, or even chewed the sides off a plank of wood so it could be used as the insert. The
animals also stacked boxes to reach suspended food, and developed a “climbing jump”
using a long stick, holding it vertically and climbing quickly before it tipped over
(Köhler, 1927).
Such behaviors imply the use of a number of cognitive faculties: Spatial processes and
memory to be sure, but possibly also planning and the understanding of causality. In this
chapter we consider the use of tools by great apes, and their development of tool cultures
through social learning. We examine the relationship between brain size and tool use, as
well as the evolution of grip. Hominin tools and tool cultures are described, and ape and
human tool behaviors are compared. Last considered are the role of planning in tool
manufacturing and the understanding of causality, and changes in the brain that evolved to
support them.
Great ape tool use

Modern research has revealed extensive tool use by chimpanzees in natural circumstances.
Beginning in the 1960s, Jane Goodall reported from the Gombe Forest Preserve in
Tanzania that chimpanzees use twigs for “termite fishing”, sticks to retrieve honey
from underground bees’ nests, and leaves as sponges (Van Lawick-Goodall, 1971).
Subsequently, a wide range of chimpanzee tools have been identified, including leaves
used as scoops, stones as hammers and anvils, and sticks as digging tools, levers, hooks,
bone marrow picks, pounding clubs, and spears (McGrew, 1992; Pruetz et al., 2015;
Sanz & Morgan, 2007).
Furthermore, not all tool uses are practical in the sense of aiding feeding or drinking. Thus,
assemblages of stone have been found inside tree hollows, thrown there by chimpanzees
during ritual-like display behaviors that include pant hoots and drumming on the tree by the
feet or hands (Kühl et al., 2016). The trees appear to be selected for their resonance at low
frequencies (Kalan et al., 2019).
Based on these observations, it seems reasonable to suppose that the chimpanzee-human
common ancestor was proficient in a limited vegetation- and stone-based tool culture
7.5 million years ago. Sticks trimmed and sharpened for insertion seem within the capabilities
of such a creature. So do sticks employed to hook otherwise inaccessible objects, leaves
wadded as sponges, and stones used as hammers and anvils.
DOI: 10.4324/9781003137863-14
Tools and planning 181
Might such capabilities have existed even earlier? If so they should be observed in other
apes. In this regard gorillas seem enigmatic, in captivity using and sometimes modifying sticks
into probes, weapons, and rakes, but almost never employing tools in the wild (McGrew,
1992; Parker, Kerr, Markowitz, & Gould, 1999). A notable exception is a female observed
using a stick as a depth-tester when wading a pool, and as a prop while collecting aquatic
plants (Breuer, Ndoundou-Hockemba, & Fishlock, 2005; see Figure 11.1).
Tool use by orangutans is rare in the wild (Byrne, 2004), but common and even creative in
captivity where it is perhaps unleashed by boredom (McGrew, 1992), or under a more
positive view, by curiosity resulting from contact with humans and conspecifics in a risk-free
environment (Damerius, Graber, Willems, & van Schaik, 2017). Nevertheless wild or-
angutans do use sticks to probe bees’ nests for honey, and to extract insects from nests and
seeds from fruit (Fox, Sitompul, & van Schaik, 1999).
The use of tools by the great apes, even if limited, might lead us to conclude that tool use is
phylogenetic. However, before we make that leap we might consider a warning by W.C.
McGrew (1992, p. 196):
Termite fishing may just as well have been invented in 1959, the year before Jane
Goodall arrived, or a million years ago. It may well have been invented only once by
some chimpanzee Edison… and then diffused across Africa, or it may have been re-
invented 100 or 1000 times.
McGrew’s point seems well taken. To what extent might primate tool use be cultural and
recent, and not phylogenetic and ancient?
Figure 11.1 Gorilla using a depth tester.

Source: Gorilla tool use.png, CC BY 2.5, Thomas Breuer, Mireille Ndoundou-Hockemba, Vicki Fishlock.
Primate tool cultures
One reason to believe primate tool use may be cultural is that different chimpanzee groups
have different tool practices. For example, after comparing sites in Africa, McGrew (1992)
noted substantial variation in chimpanzee use of the oil palm. On one hand, in Guinea, stone
anvils and hammers were employed to crack palm nuts to remove the nutritious kernels. But
in Gabon, hammers were not used and the palm fruit was consumed whole, with the un-
cracked nuts passing through the digestive system. Both contrast with the Ivory Coast, where
palm fruit was available but ignored, even though hammers were used to crack open other
nuts.
Explaining such differences is difficult based on phylogeny alone. Instead, such variations
could represent tool cultures, with some societies passing practices from one individual to
another, and with other societies failing to develop them at all.
Defining culture
Whether or not chimpanzees show evidence of culture may depend on how culture is
defined. A full definition might involve assessing a behavior’s innovation, dissemination,
standardization, durability, diffusion, and tradition, among other attributes (Davidson &
McGrew, 2005). Andrew Whiten and colleagues, however, have focused on just two
characteristics: Cultural variation, the extent to which a behavior differs between ape com-
munities, and diffusion, the extent to which behavioral similarities across communities are
attributable to social transmission (Whiten et al., 2001).
With respect to the first of these, Whiten et al. identified 39 behaviors qualifying as
cultural variants in chimpanzee communities stretching across Africa. Each variant was ha-
bitual in at least one location and absent in at least one other. While not all involved tool use
(e.g., the “rain dance”, a display at the start of heavy rain), many did (e.g., using a pestle to
pound palm crowns, or leaves to clean the body).
Diffusion, the second characteristic, is difficult to assess. As Davidson and McGrew (2005)
stated, “Processes of social transmission are extraordinarily difficult to document for animals
that cannot speak to us” (p. 806). Nevertheless, the availability of chimpanzee communities
stretching from West to East Africa allowed Whiten et al. the opportunity to identify possible
instances by examining whether contiguous communities showed similar behaviors. Of
several tool use behaviors, nut hammering was found to be consistent with a single origin
followed by diffusion to contiguous communities. Other tool behaviors were found in
noncontiguous communities and thus were more consistent with multiple origins. For ex-
ample, the use of sticks in ant dipping, clubbing, levering, and termite-fishing were judged
likely to have been invented in more than one location (Whiten et al., 2001). It is notable
that these behaviors are simpler than nut hammering, which involves assembling multiple
parts and sequencing actions. Perhaps simple behaviors are reinvented, while complex ones
tend to be invented once and socially transmitted.
Consistent with this, when naïve chimpanzees were provided with potatoes accessible only
by pounding a small opening in a container with the end of a stick, a simple behavior not
requiring sequencing or multiple parts, “stick pounding” was spontaneously invented by one
chimpanzee in each of three of four groups. No teaching was involved (Bandini & Tennie,
2019). In contrast, nut cracking, a complex skill found to develop slowly over ten years or
more, involving controlled striking of a carefully positioned nut relative to anvil and
hammer, was accompanied by active teaching of young chimpanzees by adults. Thus, a
mother might reposition a nut for a child, provide a hammer, or demonstrate the nut
cracking sequence. However, no evidence was found that chimpanzees use pointing, or
repositioning of a child’s body parts as part of their teaching repertoire (Boesch, Bombjaková,
Meier, & Mundry, 2019).
In orangutans, cultural diffusion has been reported by van Schaik and colleagues across
locations in Sumatra and Borneo. They identified 24 likely cultural variants, a number of
them involving tools (e.g., wiping the face with squashed leaves and using a stick to scratch
the body). There proved to be a pronounced correlation with distance: The closer two
locations were, the more they resembled one another with respect to cultural variants. That is
exactly the result expected of diffusion (van Schaik et al., 2003). Similar results have been
reported in gorillas (Robbins et al., 2016).
Social learning
Diffusion presumably occurs through social learning, the acquisition of new behaviors by
observing others. A detailed example was provided by a study of wild chimpanzees at Bossou
in Guinea (Biro et al., 2003). The community was already familiar with palm nuts, and
cracking with hammer and anvil was customary. When unfamiliar coula and panda nuts were
provided, it was primarily juveniles who initially undertook their cracking, although a
number of adults eventually did as well. Notably, nut-cracking attracted interest among
others, with juveniles frequently observing their peers.
Juvenile-led innovation has been observed in several other contexts, including potato and
wheat grain washing by Japanese macaques (Choleris & Kavaliers, 1999; Schofield, McGrew,
Takahashi, & Hirata, 2018). While not a general primate characteristic, it notably exists in the
social and investigative activities of chimpanzees, and in investigative uses of objects by
capuchins (Perry, Barrett, & Godoy, 2017). Yet in the Bossou study, learning how to crack
the new nuts mostly involved individuals observing their peers or older animals, not younger
ones (Biro et al., 2003). Together these observations suggest that juveniles are more likely
than adults to introduce object-related cultural innovations, but are also more often ignored.
Perhaps the combination encourages “prudent innovation” – change is allowed, but only
slowly in case of pitfalls. In any case, the parallel with the introduction of new human fads
and customs seems irresistible.
The acquisition of tool use in an orangutan was described by Fox et al. (1999). Andai, a
juvenile, often observed her mother use sticks to probe tree holes. Two years later, she made
her own tools, which she used to probe holes that her mother had just left. Two years after
that, she was a fully competent tool maker and user who found her own holes to probe.
Significantly, during the learning phase, the mother was once observed to make her probes in
an inefficient way, by shortening them on both ends rather than one end, and Andai pro-
ceeded to make a tool in the same manner.
The propagation of an inefficient technique seems a sure tip-off to its acquisition through
observational learning (Fox et al., 1999). A similar example is the imitation by younger
chimpanzees of a manually disabled adult’s inefficient technique for self-grooming, involving
rubbing against a vine held fast by the feet (Hobaiter & Byrne, 2010). Another is the adoption
by migrating female chimpanzees, of the nut-cracking techniques of their new group (e.g.,
the use of wooden hammers), even though they previously used more efficient ones (e.g., the
use of stone hammers; Luncz, Sirianni, Mundry, & Boesch, 2018).
Nevertheless social learning can be expected to more frequently spread efficient techniques
within a group than to inhibit them. Presumably this accounts for the observation that
termite fishing behaviors are more similar among members of the same group, than they are
between groups (Boesch et al., 2020). The spread of an efficient, novel tool behavior has
even been directly observed in a chimpanzee community in Uganda. A flooded waterhole
was apparently the impetus for the dominant male to craft a moss-sponge, which he then
used to drink water. Over six days, seven more chimpanzees were observed doing the same.
Six had been explicitly observed watching the male doing so, and the seventh acquired the
crafting behavior immediately after using a discarded moss-sponge (Hobaiter, Poisot,
Zuberbühler, Hoppitt, & Gruber, 2014).
Such examples represent relatively passive social learning: One individual engaged in a
behavior, and another learned by watching. Active teaching, involving one individual in-
tervening to further the learning of another, is much rarer in primates. However, it has been
seen in chimpanzees in the form of “tool transfers”. Skilled females have been observed
preparing termite-fishing probes before handing them to their child or sibling. Subsequently,
the recipient “fishes” for a longer period, with more nest insertions, than in periods before
they were handed a tool. The presumption is that at minimum, providing an expertly
prepared tool affords an enhanced opportunity to learn termite fishing. But it may also
transfer knowledge about the appropriate raw materials from which to make a probe
(Musgrave, Morgan, Lonsdorf, Mundry, & Sanz, 2016). It appears that mother-to-child tool
transfers more often occur with complex tool sets than simple ones, indicating that teaching is
more intense when greater knowledge must be imparted (Musgrave et al., 2020).
In conclusion, there can be little doubt that cultural transmission through social learning
helps spread ape tool culture. However, it seems equally clear that phylogeny must play a role
as well. First, while social learning may be widespread among animal species, apes excel at it
and may be the only animals to understand requests to “do this” (Zentall, 2006). The im-
plication is that the biologically based intelligence of apes has much to do with cultural
transmission. Second, as the Whiten et al. study indicates, and as other studies have docu-
mented, many tool behaviors are continually reinvented (Bandini & Tennie, 2017, 2019;
Laumer, Call, Bugnyar, & Auersperg, 2018). That too grounds tool behaviors in the basic
intelligence of apes. When these considerations are paired with the evolutionary changes in
praxis and handedness outlined in the previous chapter, the conclusion appears unavoidable
that primate tool use is ultimately phylogenetic – and cultural.
Brain size and tool use

The idea that intelligence engenders tool use is supported by a relationship between tool use
and brain size in birds (Lefebvre, Nicolakakis, & Boire, 2002). Across bird species, the use of
tools is associated with a larger residual brain size, which is the amount of brain over and above
that predicted by body weight. This is a concept similar to the encephalization quotient
(EQ). In birds the relationship is accounted for by the relative size of the neostriatum, one of
the brain areas believed to be equivalent to neocortex in mammals (Lefebvre et al., 2002).
However, tool use is widespread among animals, and it may not be related to brain size in all
animal groups (see Box 11.1).
Box 11.1 Tool use in birds and other nonprimates
Although apes provide the most applicable comparisons to human tool use, we now
know that many nonprimates use tools as well. Among birds, corvids (crows, ravens,
jays, magpies, etc.) show diverse tool behaviors. These include holding food with a
skewer, dropping prey on hard surfaces, using sticks to extract food from holes, and
crafting and using hooks to retrieve food ( Lefebvre et al., 2002; Rutz, Klump, et al.,
2016; Rutz, Sugasawa, van der Wal, Klump, & St. Clair, 2016).
Tool use has also been found in about 30 aquatic species, including cephalopods,
crustaceans, and fish. The use of coconut shells for protection by octopuses has been
observed, much like hermit crabs use gastropod shells as temporary housing. Hermit
crabs also sometimes carry sea anemones on the shells, using their stinging cells to
repel predators and their weight to help maintain balance. The squirting of water jets
can be viewed as tool use and is employed by many fish and squid to attack prey,
burrow, or to attach eggs. Some fish are also known to use stone or coral anvils to
crack shellfish or to remove spines from sea urchins. Others lay their eggs on leaves,
then protect them by subsequently moving the leaves from danger. Sea otters use
stone hammers and anvils to extract the meat of shellfish, and bottlenose dolphins
sometimes “wear” sponges as protection while foraging ( Brown, 2012; Mann &
Patterson, 2013).
Among tool-using terrestrial mammals are elephants, which sometimes throw
objects at others as part of aggressive displays ( Bentley-Condit & Smith, 2010), and
which modify and use branches to ward off flies ( Deecke, 2012). A brown bear has
been observed picking up a barnacle-encrusted rock in its paws, and using it to rub its
face, perhaps to relieve itching or to remove food debris ( Deecke, 2012).
Even insects have been observed using tools. Some ants use leaves as carriers for food
( Brown, 2012). Sawfly larvae defend themselves by applying tree-derived acids to their
attackers ( Bentley-Condit & Smith, 2010).
Nonprimate animals may offer fertile ground for examining the relationship
between brain size and tool use. Corvids, which we have seen show diverse tool
behaviors, are notably large-brained among birds ( Emery, 2006). On the other hand,
preliminary analysis suggests that in fish, there is little relationship between tool
use and “residual” brain size after correcting for body weight ( Brown, 2012). In the
future, determining the conditions under which brain size predicts, or does not
predict, tool use may provide further insight into the evolutionary origins of our
own tool usage.
Intriguingly, brain size also appears informative in the case of capuchins. As New
World monkeys they seem unlikely candidates for high intelligence, but nevertheless
show EQs equivalent to those of macaques (Table 11.1). Wild capuchins of both the
Sapajus and Cebus genuses use stone hammers and anvils to crack nuts (Barrett et al.,
2018). This is accomplished not with a free-fall drop of the hammer, but with a full
follow-through of the arms and shoulders, sometimes recruiting muscles of the lower
body. The behavior is known to predate provisioning by humans, using the nuts of wild
palms (Fragaszy, Izar, Visalberghi, Ottoni, & de Oliviera, 2004). Capuchins also hammer
hard-shelled fruit, seeds, crabs, and snails (Barrett et al., 2018; De Moraes, Souto, &
Schiel, 2018).
Termite fishing affords a second behavioral resemblance between capuchins and
chimpanzees. Wild capuchins have repeatedly been observed tapping a termite nest, in-
serting a stick while rotating it, and removing the stick to eat the attached termites.
Impressively, the tapping appears to have the function of rousing the termites, increasing
the yield, while the rotation reduces stick breakage. Neither of these elaborations of
technique have been reported in chimpanzee termite fishing (Souto et al., 2011).
Generally speaking, brain size fairly well predicts tool use in primates. Macaques, the
encephalization equivalent to capuchins, have been observed using hammerstones to open
oysters and, more recently, to crack palm nuts (Proffitt et al., 2018). They also use leaves to
Table 11.1 Comparative encephalization quotients (EQs) among living primates, two extinct Eocene pri-
mates, and a living, related tree shrew. mya = millions of years ago
Group Species Common name EQ
Homo Homo sapiens Modern human 64

Great apes Pan troglodytes Common chimpanzee 18
Pan paniscus Bonobo 18
Gorilla gorilla Gorilla 18
Pongo pygmaeus Orangutan 18
Lesser apes Hylobates lar White-handed gibbon 9.2
Symphalangus syndactylus Siamang 9.3
Old World Cercopithecus aethiops Vervet monkey 6.4
monkeys Macaca arctoides Stump-tailed macaque 8.3
Macaca fascicularis Crab-eating macaque 6.5
Macaca mulatta Rhesus macaque 8.1
Papio anubis Olive baboon 11
New World Aotus trivirgatus Northern owl monkey 2.7
monkeys Ateles geoffroyi Geoffroy’s spider monkey 10
Ateles panicus Red-faced spider monkey 9.5
Callithrix jacchus Common marmoset 1.9
Cebus albifrons White-fronted capuchin 7.9
Sapajus apella Black-capped capuchin 7.7
Saguinus oedipus Cottontop tamarin 1.8
Saimiri sciureus Common squirrel monkey 3.9
Strepsirrhini Eulemur fulvus Common brown lemur 2.4
Indri indri Indri 3.3
Plesiadapiforms Microsyops annectens (extinct species, 47 mya) 0.7
Ignacius graybullianus (extinct species, 55 mya) 0.4
Tree shrews Tupaia glis Common treeshrew 0.8
Note: Based on a 0.28 exponent. Homo sapiens value from Table 5.1. Microsyops brain and body masses from Silcox,
Benham, and Bloch (2010). Ignacius brain and body masses from Silcox, Dalmyn, and Bloch (2009). All other values
derived from Williams (2002), using means of male and female brain and body masses where available.
wrap and rub food items covered with thorns, stingers, or mud, and grass blades and plant
needles to floss teeth (Pal, Kumara, Mishra, Velankar, & Singh, 2018; Trébouet, Reichard,
Pinkaew, & Malaivijitnond, 2018). Spider monkeys, with slightly higher EQs, have been
reported using sticks as body scratchers (Lindshield & Rodrigues, 2009). Baboons, still higher
in EQ, throw sticks at rivals during aggressive displays (Cheney & Seyfarth, 2007, p. 187).
Perhaps we should be impressed that a gross measure of encephalization predicts as well
as it does, in that tool-relevant brain mechanisms will almost certainly be found to also vary
across species.
A final indication that EQ is related to cognitive performance, of which tool-related
behaviors are part, is afforded by a meta-analysis performed by Deaner, van Schaik, and
Johnson (2006). Using the results of previous studies, they derived a global measure of in-
telligence for each of 24 primate genuses. The measure was based on the abilities to detour,
problem-solve, learn, sort, delay response, and use tools, among others. Across 13 genuses in
Table 11.1 for which both the learning and EQ measures are available, the measures correlate
at a whopping r = .87 level. Genuses with higher EQs show higher cognitive performance.
In summary a case can be made that in primates at least, tool use is influenced by a species’
general intelligence and that this is related to encephalization. As we saw in Chapter 10, an
additional role is played by the evolution of specific brain mechanisms relative to praxis. But
as the next section outlines, the physical hand itself is a third factor affecting the evolution of
tool use and manufacture.
Figure 11.2 Orangutan using a precision grip involving the forefinger and thumb tip.
Source: Orangutan using precision grip.jpg, CC BY-SA 4.0, William H. Calvin.
The evolution of grip

Precision grip refers to the delicate holding of a small object between the index finger and
thumb. Noting that anthropologists in the 1950s and 1960s thought precision grip was a
human characteristic, Pouydebat, Coppens, and Gorce (2006) set out to determine the extent
to which it is possessed by other primate species. What they found was startling. Given the
opportunity to pick up small objects, not only humans but apes, Old World monkeys,
and even New World monkeys used precision grips a significant proportion of the time.
Furthermore, Old World and New World monkeys used it more often than apes, with the
result that nonhuman species noted for frequent tool use (i.e., chimpanzees, orangutans, and
capuchins) did not adopt precision grips more often than others.
Nevertheless, our precision grip differs from that of many other primates. We pinch an
object between the pads of our thumb and index finger, a fully opposable grip. Many other
primates have a partially opposable grip, using a side or tip of a digit as part of it
(Figure 11.2). At least in part, this is due to the animals having long fingers and short
thumbs (Drapeau, 2015).
There can be little doubt that a fully opposable thumb played an important role in our
acquisition of complex tool use and manufacture. Strictly speaking, however, it is not
unique to humans. Baboons and geladas have been observed making pad-to-pad grips, and
it is said to be an ability of most terrestrial cercopithecines, a classification that also includes
macaques (Marzke, 1997). What may make it seem unique is that it is not a characteristic of
other apes (Almécija, Shrewsbury, Rook, & Moyà-Solà, 2014; Marzke, 1997; Pouydebat
et al., 2006). If a relatively long thumb is required, that condition at least may have first
appeared in our direct ancestral line about 10 million years ago in our common ancestor
with gorillas (who as apes go, are long-thumbed). In that case the short thumb of the other
great apes is a derived character reflecting below-branch suspension (Almécija, Smaers, &
Jungers, 2015; Drapeau, 2015).
Human hand dexterity

When thinking about our ability to use tools, it is useful to consider the overall dexterity
of the hand in adopting a range of grips and postures. Marzke and Marzke (2000) noted
that the ability to cup the hand around objects of different shapes seems to be a speci-
fically human capability. Such dexterity is thought to be in part the product of distinctive
hand joints and bone surfaces. Because we have the highest ratio of thumb length to
index finger length of any primate, we also better accommodate different shapes and can
rotate them between thumb and fingers. In addition, the pads at the ends of our fingers
are uniquely stabilized at their tips but mobile elsewhere, allowing conformation to
different shapes.
Another distinction is that humans have a horseshoe-shaped crest on the distal segment of
the thumb as well as a small round bone embedded in the tendon attached to it. Both features
greatly increase the leverage the tendon can exert, improving the thumb’s gripping power
(Marzke & Marzke, 2000). Indeed, humans can exert considerable force in “precision pinch”
grips, while other primates cannot. Their grips might instead be called “precision holding”
(Tocheri et al., 2003).
Homo habilis had the aforementioned tendon bone, as well as broad fingertips and a wrist
suggesting a fully opposable thumb. As a result, stones would have been held in a strong,
stable grip (Marzke & Marzke, 2000). In fact the changes probably began earlier than that.
Analyzing the distal thumb segment of Orrorin tugenensis, Gommery and Senut (2006)
concluded that it possessed the horseshoe-shaped crest identified by Marzke and Marzke
(2000) as the attachment point for a tendon capable of high leverage. If so, the fossil extends
the evolutionary history of a powerful thumb back to six million years ago.
Nevertheless, subsequent change made the human grip even stabler and more forceful.
The metacarpal bone of the thumb, the long bone nearest the wrist, developed a flatter head
that made its farther joint act like a hinge, reducing the joint’s range of motion and producing
a firm grasp. This shape change was not yet visible in Australopithecus afarensis (lived 3.0 to
3.7 million years ago); existed in an intermediate state in Australopithecus africanus, sediba, and
robustus/early Homo (collectively 1.0 to 3.0 million years ago); and was essentially complete in
Homo naledi and neanderthalensis (collectively 40,000 to 400,000 years ago; Galletta, Stephens,
Bardo, Kivell, & Marchi, 2019). Recent biomechanical modeling has reinforced these
conclusions by revealing that two million years ago, australopithecines had a less forceful
precision grip than later Homo sapiens and Neanderthals (Karakostis et al., 2021).
The earliest hominin tools

Vegetation must have accounted for much of the toolmaking material employed by the
earliest hominins. Primate tool cultures commonly show use of twigs and sticks as probes,
levers, hooks, spears, and digging tools, and of leaves as sponges and scoops. These were
almost certainly within our ancestors’ capabilities after they split from the chimpanzee line.
Fossil evidence may never be found, however, because such tools would not have been
cached in quantity, and vegetation usually decays rapidly.
Chimpanzee observations suggest that the earliest hominin tools made of permanent
materials were probably natural stones used as hammers and anvils. In fact hammers and anvils
up to 3.3 million years old have been identified from sites near Lake Turkana in Kenya
(Arroyo, Harmand, Roche, & Taylor, 2020; Harmand et al., 2015). Hominin hammers and
anvils have also been discovered at Olduvai, dating to about 1.8 million years ago (Diez-
Martin et al., 2010).
Traditional tool use among modern-day Australian hunter-gatherers provides potentially
valuable insights into other early hominin tools. When the Australian hunter-gatherers use
stone tools, it is primarily to make wooden objects such as spears and digging sticks. Sharp
edges are taken as they come: As natural edges if available, but as flakes broken off stone cores
if not. Flakes with a right-angle edge are used to smooth surfaces on shaft tools like spears.
Although worn flakes are sometimes resharpened, more often new flakes are selected. All of
these kinds of tools would be very difficult to identify in archaeological contexts. They have
unworked edges for the most part, and the casual nature of their acquisition scatters them
across sites (Hayden, 2015).
Worked stone tools

The earliest known hominin tools made of worked stone, like the earliest possible hammers
and anvils, come from near Lake Turkana. Consisting of cores and flakes, their working is so
crude that a naïve eye might not recognize them as tools. Nevertheless, there is evidence for
transportation from a raw material site 100 meters away, and for multiple fractures of stone
from cores. At 3.3 million years old, they substantially predate the genus Homo. Either
Australopithecus afarensis or Kenyanthropus platyops is considered their likely maker (Lewis &
Harmand, 2016), although some have questioned whether sufficient grip force could be
generated by the afarensis hand during tool manufacture (Domalain, Bertin, & Daver, 2017).
They have been termed Lomekwian tools after the site at which they were found, in re-
cognition of distinctive fracturing and their status as an apparent waypoint between pounding
and flaking technologies (Harmand et al., 2015).
Gona and Oldowan tools

The next oldest tools are 2.6 million years old. They were found at Gona, Ethiopia, and were
possibly crafted by Australopithecus garhi. They have been described as “cores, whole and
broken flakes, angular and core fragments, a small number of retouched pieces and in some
instances unmodified stones transported to sites” (Semaw, 2000, p. 1198). Flakes pre-
dominate, not only for the obvious reason that multiple flakes must be struck from a core to
make it into a tool, but because obtaining the sharp-edged flakes themselves would often
have been the maker’s object. The flakes show swellings just below the point of impact that
clearly indicate human agency. Some cores show pitting consistent with use as hammer-
stones, although that can also occur from weathering. To the less-trained eye, however, it is
the flaked tools that are most identifiable as produced by hominins (Figure 11.3, especially
the right and bottom views showing multiple removals).
More controversially, stone tools have been reported in Jordan dating to 2.5 million years
ago. If true, the implication is that hominins first left Africa by that date (Scardia et al., 2019).
However, some are skeptical that the stones were tools, and suggest they were naturally
chipped by being thrown together in water (Kemeny, 2019).
Figure 11.3 Views of a tool from Gona, Ethiopia.

Source: Pierre taillée Melka Kunture, Ethiopia fond.jpg, CC BY-SA 4.0, Didier Descouens.
The Gona tools resemble the Oldowan toolkit, named for Olduvai Gorge in Tanzania
where 1.9 million-year-old tools were found and attributed either to australopithecines or to
Homo habilis. In recent years, however, Oldowan-like tools have also been found in the
Republic of Georgia in Eurasia. They date to about 1.8 million years ago (Mgeladze et al.,
2011). They are thought to have been produced by Homo erectus. Assemblages of Oldowan
tools, dating to 1.3 to 1.6 million years ago, have also been found associated with Homo erectus
crania in Ethiopia (Semaw et al., 2020).
Roughly contemporaneous with some of the older tools are cut marks on bone, from
Bouri, Ethiopia, dating to 2.5 million years ago. Hammerstone impact marks on a shattered
bovine tibia also indicate the extraction of bone marrow. These discoveries are from layers
associated with fossil remains of Australopithecus garhi, suggesting that it was the toolmaker
(de Heinzelin et al., 1999). A claim of even earlier cut marks dating to 3.4 million years
ago (McPherron et al., 2010), was initially criticized on the basis that they may have
resulted from trampling (Domínguez-Rodrigo, Pickering, & Bunn, 2010). However, the
claim has been made plausible by the subsequent reporting of actual stone tools from 3.3
million years ago, and studies indicating that trampled bones do not show similar cut marks
(Thompson et al., 2015).
That early hominin tool kits were effective in allowing the consumption of meat and
marrow is suggested by an analysis of carnivore extinctions in East Africa (Faurby,
Silvestro, Werdkin, & Antonelli, 2020). Large carnivores underwent progressive ex-
tinction there, from four million years ago to the present time. As the researchers pointed
out, the beginning of the decline corresponded to the first achievement of hominin brain
volumes above 500 cc, and indeed, the first EQs over 20 (see Table 5.1). The pre-
sumption is that increasing intelligence, and an increasingly effective toolkit, allowed
hominins to compete with large carnivores, either through direct hunting, scavenging, or
the stealing of kills. Importantly, this effect was not seen in small African carnivores, or in
carnivores in North America, where hominins were absent until recently. Competing
hypotheses, such as changes in climate or forest cover, also did not account for the effect
(Faurby et al., 2020).
The role of cognition

Did worked stone tools originate 3.3 to 3.4 million years ago in a sudden flash of insight that
spread through cultural means? Or did they emerge more gradually? It is too early to tell, but
either way it seems safe to assume that vegetation-based tools long preceded worked stone.
Apparently a lengthy period of evolution was necessary to bridge the conceptual gap between
stick tools and worked stone tools. Yet if strong grips emerged early, possibly in Orrorin six
million years ago, and hunting even earlier, then the gap was apparently not related to shifts
in grip or diet. The conclusion seems inescapable that something cognitive occurred at the
time of the australopithecines that allowed a transition from vegetation-based and natural
stone tools to worked stone tools.
A clue to that “something” comes from an attempt to teach knapping (shaping stone
through systematic chipping) to a captive pygmy chimpanzee named Kanzi. When striking
off flakes using a bimanual technique, Kanzi appeared not to calculate striking angles or to
have an idea of what should be accomplished (de Beaune, 2004). In other words, Kanzi
may not have been able to generate and sustain a mental model of a stone tool and how it
is formed.
Such a model would include the idea that overlapping chip removals, struck at the proper
angle off a prepared core, leave a nearly continuous, extremely sharp edge. Forming that idea
requires a high degree of three-dimensional spatial processing, and probably spatial imagery.
It seems qualitatively different, in part because of its complexity but also because the end
result is less immediate, from the spatial processing required to prepare any chimpanzee tool.
Perhaps it is a shift in spatial ability and spatial memory that we should look to for causes of
the transition to worked stone, a theme visited in the next chapter.
Alternatively, it may be that the ability to mentally order the necessary chip removals – i.e.,
planning – was more important. Even the intention to make worked tools involves planning,
because the necessary materials must first be gathered. In the case of Oldowan tools,
matching the type of selected rock to available outcrops indicates that raw materials were
sometimes transported over distances in excess of 10 km. Furthermore they were probably
selected for the durability of tool edges (Braun, Plummer, Ferraro, Ditchfield, & Bishop,
2009). That is surely a testament to the planfulness of the tool makers.
Later tools
Tools evolved much as species did, with more successful ones replacing less successful ones.
In general, later stone tools are characterized by increasing complexity and diversity.
Acheulean tools
After Lomekwian and Oldowan tools, the next tool culture to arise was the Acheulean, be-
ginning about 1.8 million years ago (Table 11.2) and named for the archaeological site of St.
Acheul in France. Handaxes first arose in this culture (Kooyman, 2000). The Ethiopian sites
where Oldowan tool assemblages are found, also host Acheulian tools in the 1.3 to 1.6
million-year-old range, and are likewise associated with Homo erectus (Semaw et al., 2020).
However, caution should be observed when identifying particular tool industries with
particular periods of time, because the period during which an industry existed depends on
the geographic location. Nevertheless it is useful to give approximate dates, as in Table 11.2,
in order to interpret other cultural remains (e.g., artwork, needles, and hearths) associated
with the cultures.
The names of the tool cultures generally reflect the geographic locations from which they
were first or best known. Thus, the Oldowan industry is named for the Olduvai Gorge in
Tanzania. Nevertheless, it should not be assumed that an industry is found only in the lo-
cation for which it was named, because most spread widely. As for why the Lower, Middle,
and Upper Paleolithic periods are so named, “think dig”. When digging down, the upper
layers are the youngest, the middle layers are the next youngest, and the lower layers are the
oldest.
Acheulean tools originated in Africa, where they are first known from 1.8 million years
ago (Diez-Martin et al., 2015; Lepre et al., 2011). However, they spread widely throughout
Africa, Europe, and Asia as far as India and Korea (Gowlett, 1992b). There is evidence that
the spread was literal, because variability in the tools is highest in Africa and lowest in areas
furthest from Africa, exactly as one would expect from transmission through repeated mi-
grations (Lycett & von Cramon-Taubadel, 2008).
These tools were substantially more complex than their predecessors, incorporating
symmetry around one or two axes, and were often heavily worked so that little or no raw
stone surface was left exposed (Gowlett, 1992a; Kooyman, 2000). When Acheulean tools
from a particular location are compared over time, skill is found to increase over hundreds of
thousands of years, improving both symmetry and the straightness of edges (Shipton, 2018).
The high degree of symmetry of some later Acheulean handaxes strikes many modern
viewers as quite beautiful, appealing to an aesthetic that their makers may have felt as well
(Figure 11.4). Yet they were also efficient tools, probably notably more efficient at butchery
than the previously used stone flakes (Galán & Domínguez-Rodrigo, 2014). Because such
highly symmetric tools are not produced in modern experiments that randomly remove
Table 11.2 Some prominent tool cultures, with very approximate ages and geological periods (kya =
thousands of years ago). Ages largely derived from Gowlett (1992b) and Jones, Martin, and
Pilbeam (1992)
Industry Approx. age Period
Lomekwian 3300 kya Lower Paleolithic

Oldowan 1000–2600 kya Lower Paleolithic
Acheulean 150–1800 kya Lower Paleolithic
Mousterian 15–150 kya Middle Paleolithic
Aurignacian 27–40 kya Upper Paleolithic
Gravettian/Périgordian 12–27 kya Upper Paleolithic
Solutrean 18–21 kya Upper Paleolithic
Magdalenian 12–17 kya Upper Paleolithic
Hamburgian/Ahrensburgian 8–13 kya Upper Paleolithic
Clovis 8–12 kya Upper Paleolithic
Figure 11.4 Acheulean handaxe from Spain.

Source: Bifaz en mano.jpg, CC BY-SA 2.5, José -Manuel Benito Álvarez.
protrusions from a core, there is good reason to believe that top-down, planful processing
was employed during their manufacture (Moore, 2020).
One late development in the Acheulean tradition was the Levallois technique, involving
removing many flakes from a core in preparation for striking off one desired flake that with
minimal or no retouching (secondary flaking along the edge) became the sought-after tool
(Gowlett, 1992b; Figure 11.5).
The advantage to this technique was that through careful preparation of the core, a tool
exactly the desired size and shape could be obtained, with a sharper edge than was possible
using earlier techniques (Kooyman, 2000). Achieving this provides another instance of the
use of top-down, planful processing (Moore, 2020).
What Acheulean tools were used for, besides butchery, has been a point of con-
troversy. However, analysis of phytoliths (microscopic mineral particles formed by plants)
found on the working surfaces of Acheulean handaxes from about 1.5 million years ago
indicate that they were used for chopping wood (Dominguez-Rodrigo, Serrallonga,
Juan-Tresserras, Alcala, & Luque, 2001). The finding is important in revealing that
woodworking occurred at a remote time from which wooden artifacts themselves have
Figure 11.5 Levallois technique, showing the desired flake removed from the core.
Source: Adaptation of Production of points & spearheads from a flint stone core, Levallois technique, Mousterian Culture,
Tabun Cave, 250,000–50,000 BP (detail).jpg, public domain, Gary Todd.
not survived. However there is also evidence that points of Acheulean age, in this case
500,000 years ago, were hafted to shafts to make spears, becoming the first known in-
stances of composite tools (tools made of more than one material). Presumably they were
used for hunting (Wilkins, Schoville, Brown, & Chazan, 2012). The varied uses of the
Acheulean handaxe have led to its being described as the “Swiss army knife” of its age
(Calvin, 2002).
While surviving Acheulean tools are almost always made of stone, recent analyses of ar-
tifacts recovered from Acheulean sites in the Olduvai Gorge show that a tiny percentage
were made of bone. Most were apparently used as stone reworkers, anvils, choppers, or
cutting tools, One, however, was in the shape of a hunting point with three barbs, It was in
excess of 700,000 years old, the earliest bone point known, and was mostly likely made by
Homo erectus (Pante, de la Torre, d’Errico, Njau, & Blumenschine, 2020).
Mousterian tools
The Mousterian toolkit, named for Le Moustier, France, is largely though not exclusively
associated with Neanderthals. The emphasis was on discoids and on Levallois flakes
used as scrapers. Small stone points with true tangs, suggesting hafting onto a shaft,
developed out of this tradition and are found in northwest Africa, dating to about 22,000
to 45,000 years ago (Gowlett, 1992b; Straus, 2001). Also, arrow points made of bone,
more than 60,000 years old, have been reported in South Africa. They are thought to
have been inserted in a shaft and secured with a wrapped collar (Backwell, d’Errico, &
Wadley, 2008).
Aurignacian tools
Aurignacian culture, which extended from Spain to Russia (Gowlett, 1992b), was marked
by an increase in microblades (small blades less than 5 cm in length) and microliths (small
blades with at least three distinct sides). The latter were mounted in series to form a
continuous edge. By thus combining stone with a mounting material, a composite tool was
created (Kooyman, 2000). Aurignacian culture also created bone points. Bone and antler
were common toolmaking materials although wood was undoubtedly used as well
(Gowlett, 1992b).
Gravettian and Solutrean tools

Gravettian culture (called Périgordian in France) was characterized by backed blades (blunted on
one edge, probably for ease of use; Figure 11.6) and the common utilization of scrapers
(Gowlett, 1992b).
The co-occurring Solutrean culture achieved the most sophisticated of all Paleolithic stone
tools, the laurel-leaf point, named for its characteristic shape (Figure 11.7). It was made by
pressure-flaking, in which flakes are detached by pressure rather than with blows, re-
presenting another technological advance (Gowlett, 1992b; Kooyman, 2000).
Figure 11.6 Reverse sides of a backed blade.

Source: Adaptation of Neolithic Backed Blade (FindID 661331).jpg, CC BY-SA 2.0, by North Lincolnshire Museum,
Martin Foreman.
Figure 11.7 A Solutrean laurel-leaf point.

Source: Biface feuille de laurier.JPG, public domain, Calame.
Figure 11.8 Magdalenian bone needle.

Source: Adaptation of Aiguille os 246.1 Global.jpg, CC BY-SA 4.0, by Didier Descouens.
Magdalenian tools
Magdalenian culture introduced harpoons, lance-heads, and spearthrowers, made from bone and
antler. The spearthrowers were often decorated with carvings of animals, birds, and fish. Bone
needles, complete with eyes, attest to the wearing of clothing (Clark, 1967; Gowlett, 1992b;
Figure 11.8), although the invention of clothing must have substantially predated this culture
(see Box 11.2). Microlithic backed stone blades were also common (Kooyman, 2000).
Box 11.2 The great denudation
Important tool uses have included the preparation of hides and textiles for clothing and
shelter, and the creation of fire. To some extent, these thermoregulatory uses of tools
must be linked to the reduction of body hair in the hominin line, or in other words to
what Markus Rantala has picturesquely called “the great denudation”. While the
density of hair follicles does not differ significantly between humans and other apes,
hair size does, and as a result humans have nakeder skin. Thus, in our ancestry there has
been hair loss that can be characterized as a reduction in coat thickness ( Rantala, 2007).
In the past there has been little consensus on whether the use of clothing, fire, and
portable shelters accompanied the loss of hair, or followed it much later as hominins
moved into colder climates. To begin addressing this question, Rogers, Iltis, and
Wooding (2004) examined changes in the MC1R gene. The gene affects skin color
and was selected on the assumption that the loss of body hair must have been
accompanied by darkening skin as protection against the sun. Using a molecular-clock
approach, the researchers concluded that the great denudation occurred about 1.2
million years ago. Interestingly, this date corresponds to a split in the human louse line,
with different subspecies of lice beginning to diverge at about that time ( Light & Reed,
2009). Certainly the loss of human body hair would have had implications for body
parasites.
But at what point was clothing adopted? Based on a later genetic divergence
between human head lice and body lice, it has been argued that clothing first appeared
83,000 to 170,000 years ago. Thus, the much earlier denudation is assumed to have
confined lice to the head, which then moved to the body and genetically diverged
once clothing was adopted. The 83,000 to 170,000-year-old date is believed to be
prior to the first permanent passage of modern human beings into Europe, suggesting
that clothing was invented before the successful removal of Homo sapiens to cold
climates ( Toups, Kitchen, Light, & Reed, 2010). However, this leaves unclear how
earlier hominins were able to survive in the cool parts of Europe before 500,000 years
ago ( Hosfield, 2016).
Direct evidence of clothing is very limited beyond a few thousand years ago. The
oldest known clothing dates back 20,000 years, and dyed flax fibers about 33,000 years.
Less direct evidence includes eyed needles at 30,000 to 35,000 years, and bone awls at
76,000 years or more ( Hoffecker, 2005; Kvavadze et al., 2009; Rantala, 2007).
Although scraped hides likely extend back about 300,000 years ( Kvavadze et al.,
2009; Rantala, 2007), hides can be used for either clothing or shelter ( Toups et al.,
2010). If they were then used for clothing, it may have been in a simple form involving
draping a single layer loosely over the body, providing only a small amount of warmth.
Complex clothing, consisting of fitted pieces sewn together to more tightly fit the
arms, legs, and torso, might then be inferred from the much later awls and needles.
They would have been warmer, and they would have allowed layering for even greater
warmth ( Gilligan, 2010). Perhaps it was this form of clothing that appeared 83,000 to
170,000 years ago.
The material evidence relating to the use of fire is also limited. In Africa, it may
date as far back as Homo ergaster or erectus 1.5 to 1.7 million years ago. Yet a heating
purpose cannot necessarily be assumed because fire can also be used for light,
protection against predators, cooking, and socializing ( Beaumont, 2011; Gowlett,
2016). Although there is some evidence from an Israeli site that fire was used to roast
grains and fruit 780,000 years ago ( Melamed, Kislev, Geffen, Lev-Yadun, & Goren-
Inbar, 2016), in colder European climates there is no evidence of any intentional use
of fire until after 450,000 years ago ( Roebroeks & Villa, 2011). Thus, the story of
the great denudation, and its implications for clothing, shelter, and heating in colder
parts of the world, is likely to prove a complicated one to unravel.
Hamburgian and Ahrensburgian tools

The Hamburgian and Ahrensburgian cultures are known for their many organic remains,
preserved in both caves and open-air sites. Analysis of animal remains and projectile points
yields the conclusion that Hamburgian hunters shot animals (usually reindeer) from the side,
often while a herd passed through a valley entrance. Some debate remains whether spear-
throwers or bows and arrows were used, but evidence leans toward the former, at least until
the later Hamburgian period. The somewhat later Ahrensburgian culture definitely had
arrows as is known from the remains of their notched shafts (Terberger, 2006).
Clovis tools
Finally, the Clovis culture is specific to central North America and is named for a site near
the town of Clovis, New Mexico. It is known for elaborately worked stone points with a
fluted base that allowed firmer attachment to a shaft. Clovis hunters took down large game
including mammoths, mastodons, camels, and bison (Gowlett, 1992b; Waguespack &
Surovell, 2003).
Comparison of ape and human tool behaviors

With respect to tool use and manufacture, what humans and other apes may have in
common is the ability to create, remember, and execute a script. This can be defined as a
contextually-dependent series of actions leading to a goal. For instance, a nut-cracking
script might involve searching for a hammer, transporting it to an appropriate site, locating
an anvil, bringing nuts to the anvil, cracking the nuts between the hammer and anvil, and
consuming the nuts. Observations of ape tool use clearly show an ability to follow such
scripts, not just in nut-cracking but in the preparation of “fishing” tools, hunting spears,
leaf sponges, and honey probes (Parker, 2004). Scripting is also implied when apes use
more than one tool in sequential order, as in the use of a stick to penetrate underground
termite nests, followed by application of a frayed “brush tip” probe to fish for the insects
(Musgrave et al., 2020).
Where humans and other apes differ is in script complexity. We can incorporate more
steps in the sequence of actions needed to reach the goal, and in the number of alternative
actions accommodated during the sequence (Parker, 2004). This notion of a human-ape
difference in script complexity is related to the qualitative differences, already highlighted, in
the planning and spatial processing humans and apes bring to toolmaking. Stone tools require
more steps than simple vegetation-based tools, increasing both the complexity of the script
and its memory demands. Even the production of relatively crude Oldowan tools involves as
many as 11 different cognitive decisions, such as selecting a hammer, selecting a core,
choosing a point of impact, and modulating the force of impact. Acheulean tools, the next
step up in complexity, involve as many as 46 decisions, many of them arranged hierarchically
and repetitively (Toth & Schick, 2019).
Similar differences in planning and execution over time are seen in two other aspects of
human tool manufacture (Byrne, 2004). First, composite tools, made from multiple com-
ponent parts, are found in all known human cultures and indicate planning for assembly.
Second, humans manufacture many tools whose sole use is to make or assist other tools, the
ultimate in long-term planning. Add to these elaborations the wide diversity of materials
used by humans, and animal tools seem “poor things in comparison” (Byrne, 2004, p. 32).
A likely reason for that is that apes lack the degree of memory-intensive spatial planning
needed to seek diverse materials, transform them by way of protracted processes, and if
necessary combine them into composite tools.
Increased hominin planning

An increase in hominin planning appears to have emerged by at least 2.6 million years ago.
Although Oldowan tools seem simple to us, possibly even within the grasp of a nonplanning
mind, meticulous reconstruction of Oldowan cores from their constituent flakes implicates a
manufacturing process in which up to 30 flakes were struck off in sequence. Furthermore,
strike angles were maintained throughout the sequence, and the technique was repeated
across cores (Byrne, 2004).
Other data, derived from later Acheulean examples, show that stone tools were rarely
completed in one location. Instead a core might be produced at one place through initial
flaking, then removed to a second place for further flaking (Hallos, 2005). This shows a
striking resemblance to modern adze-making on the island of New Guinea. Adze-making
involves knapping rough forms at a quarrying site, followed by transportation to a village
and then more detailed stonework (Stout, 2002). Such operations extend the time frame
over which the overall goal must be remembered and over which subgoals are attained
(Hallos, 2005).
There seems nothing of similar complexity in ape behavior, even if it is true that chim-
panzees engage in a limited degree of planning when they prepare a “fishing” tool at one site
for transport to another (Byrne, 2004). In fact, even lemurs, removed from humans by some
68 million years of evolution, show evidence of planning when they grasp objects with an
uncomfortable grip, in anticipation of rotating them to a more comfortable end position
(Chapman, Weiss, & Rosenbaum, 2010). But both of these behaviors represent much
simpler planning than is involved in stone tool manufacture.
Is the evolutionary emergence of complex tools yet another manifestation of increasing
brain size? The makers of the first known stone tools are thought to have been
Australopithecus afarensis or Kenyanthropus platyops. The encephalization quotient of the
latter is unknown due to an unknown body size, but afarensis had an EQ of 23 (see
Table 5.1). Interestingly, Homo floresiensis, the diminutive hominin popularly known as
“the Hobbit”, had a very similar EQ of around 25, and it too manufactured stone tools
(Morwood & Jungers, 2009). These EQ values are distinctly larger than those for the great
apes (Table 11.1).
However, raw encephalization tells only part of the story. As it turns out, the brain of
floresiensis may offer a unique insight into human advances in planning.
Brain mechanisms of planning

In hominins, traces of brain structure are often left behind on the inside surfaces of fossilized
skulls, having been impressed by pressure into developing bone. They can be recovered by
creating an endocast, either a physical latex rubber molding of the inside of the skull or a
virtual representation constructed by computational means using imaging data. Comparison
of virtual endocasts with the brains of modern humans finds that endocasts, though less
detailed, do reflect both structures and shapes of the frontal, temporal, occipital, and inferior
parietal lobes of the brain (see Figure 6.3). The correspondence is reduced for the superior
parietal lobes (Dumoncel et al., 2020).
A remarkable virtual endocast has been recovered in the case of the Hobbit. One of its
most noticeable features is a large bulge on each side of the midline at the frontal pole
(foremost part) of the frontal lobe (Figure 11.9), much more pronounced than in the modern
human brain. The location corresponds to Brodmann area 10 in our prefrontal cortex (see
Figure 10.4), which has both a lateral extent (i.e., to the side of the midline), and a medial
extent (i.e., on the inner surface of each hemisphere). It appears safe to conclude that flor-
esiensis had a relatively enlarged area 10 (Falk et al., 2005).
Why is area 10 particularly prominent in this species? We saw in Chapter 5 that floresiensis
may represent an instance of island dwarfism, the body size reduction that sometimes occurs
due to resource limitations on isolated islands. A possibility is that area 10 is enlarged in the
Hobbit because it was relatively preserved when brain size shrunk in company with shrinking
body size. Such preservation might occur if area 10 was so critical to the species’ survival that
it underwent positive selection during the dwarfing process.
The rise of area 10

That area 10 played an important role in hominin evolution is strongly suggested by
comparative analyses undertaken by Katerina Semendeferi and colleagues (Semendeferi,
Figure 11.9 View of the floresiensis endocast from the (a) side, (b) back, (c) front, and (d) top. Note the
substantial bulges, labeled as feature 6, at the frontal pole.
Source: Virtual endocast of LB1, licensed from Elsevier under STM Permissions Guidelines.
Armstrong, Schleicher, Zilles, & Van Hoesen, 2001). They found that humans have a
greatly enlarged area 10, comprising 1.2% of brain volume compared to 0.5% to 0.7% in
the great apes and only 0.2% in gibbons. Combining these findings with other data,
Semendeferi et al. proposed that in an initial ancestral state now approximated by gibbons,
area 10 occupied a limited area nearest the eyes. This was then followed by two expan-
sions: One in a common ancestor of great apes and humans, and the other more specifically
in humans when area 10 greatly expanded in size and connectivity with other brain areas
(Semendeferi et al., 2001). In concert with this, area 10 matures more slowly than other
brain areas in both chimpanzees and humans, and more slowly in humans than in chim-
panzees (Teffer et al., 2013).
The expansion’s nature is clarified by the discovery that while area 10 comprises 1.2% of
our brain volume, it has only 0.3% of the brain’s neurons (Barton & Venditti, 2013). That
means there must be unusually profuse connections between area 10 neurons, taking up
volume that might otherwise be filled by cell bodies. Indeed, pyramidal cells in area 10 are
found to have larger dendritic arbors (the treelike branchings of dendrites) relative to several
comparison areas (3, 18, and 4; see Figure 10.4 for these areas). The same is also true of
chimpanzees (Bianchi et al., 2013). It appears, therefore, that area 10 has long been under
selective pressure for increased cellular interconnectivity, going back at least to the
chimpanzee-human common ancestor.
The cognitive role of area 10
If area 10 expanded in connectivity during ape evolution and in size during hominin evo-
lution, we might expect that it serves a critically important role in cognition. In fact that
appears to be true. For one thing it is involved in human working memory, a form of memory
that holds and manipulates information over the short term. Thus, a review of brain-imaging
studies found that working memory activates the lateral portions of area 10 (Gilbert et al.,
2006). While other cortical areas may play an overall larger role in working memory (Cabeza
& Nyberg, 2000), area 10 more specifically evaluates its contents (Leung, Gore, & Goldman-
Rakic, 2005). In addition the anterior portion of the area is involved in rapidly switching
between tasks (Gilbert et al., 2006). Consistent with that, it appears to play a role in eval-
uating alternative goals and then allocating cognitive resources accordingly (Mansouri,
Koechlin, Rosa, & Buckley, 2017).
The role of area 10 in evaluating the content of working memory and in task switching has
clear applicability to the manufacturing of stone tools. Knapping involves keeping in mind a
goal state, evaluating the emerging tool in terms of that state, and repeated switching between
evaluative and action-oriented phases. The area 10 processing load would have been parti-
cularly demanding in a small-brained species like floresiensis (and perhaps not in modern large-
brained knappers, as suggested by the silence of area 10 in the brain imaging results of Stout,
Toth, Schick, & Chaminade, 2008). Together, the evaluation and task switching functions of
area 10 seem almost synonymous with planning, if planning is understood to include not just
the initial plan but its updating over time.
Other brain-imaging research confirms a role of area 10 in planning. In human experi-
ments, the Tower of London task is one of the most commonly used planning tasks, in-
volving moving beads one-at-a-time to transform a beginning state to a desired goal state
(Figure 11.10). Problems vary in complexity, e.g., from one to seven moves. While area 10
activation is not always apparent overall when the task is performed (Boghi et al., 2006),
research usually finds that its activation increases with increasing difficulty (Schall et al., 2003;
van den Heuvel et al., 2003). Also, better performance is associated with increased activation
in the area (Unterrainer et al., 2004). Both findings indicate area involvement in the task.
Further supporting the role of area 10 in planning, Roca and colleagues found that damage
to it impaired the ability to multitask while operating a virtual hotel; specifically, to perform
several subgoals while keeping in mind an overall goal. Patients with damage elsewhere in the
brain had less difficulty (Roca et al., 2011).
Figure 11.10 A three-move Tower of London problem.

It has been pointed out that area 10 is probably involved in some other functions as well:
E.g., emotion (Gilbert et al., 2006), alertness (Coull, Frackowiak, & Frith, 1998), evaluating
the implications of pain for behavior (Peng, Steele, Becerra, & Borsook, 2018) and “men-
talizing” or theory of mind (i.e., ascribing mental and emotional states to others; Gilbert et al.,
2006). Nevertheless, its involvement in planning, shown not just in working memory, task
switching, and multitasking research but in a task of a sequential nature, argues strongly for
its role in the manufacturing of tools. That the area was apparently preserved during the
reduction of the Hobbit’s brain testifies to its importance to hominins.
Understanding causality
Much of the planning using area 10 may only involve heuristics (rules of thumb that tend
toward the solution of a problem). The similarity heuristic, for example, entails making the
current state more similar to the desired end state. Followed to its conclusion, this often
results in a correctly crafted tool or a solved Tower of London problem. However, more
complex problem solving can be achieved if an understanding of causality is also brought to
bear. For example, in some of the more complex Tower of London problems, a move must
be made that decreases the similarity between the current and end states, in the interest of
allowing future moves that will again increase similarity. This requires understanding causal
relationships across multiple moves: “If I do this, then I can do that and that”.
Wolpert (2007) has argued that compared to us, apes have a very limited notion of
causality. To be sure, they can learn to associate an action with an outcome, but often lack
insight into why one leads to the other. Thus, Wolpert cited work by Povinelli, Reaux,
Theall, and Giambrone (2000) indicating that a chimpanzee may understand that tool
contact is necessary to reach food, but not understand that a hook at the end of the tool can
be used to pull the food within reach. Also, when raking food toward them with a pit
obstructing the path, few chimpanzees reliably select a pathway that avoids the food falling
into the pit. These failures suggest a very limited understanding of causality. Yet Wolpert
(2007) did allow that there is occasionally some understanding, “at the edge, even just over
the edge” as he put it (p. 59), as in the assembly of hammers and anvils and the leveling of
the anvils for nut-cracking.
The same “just over the edge” conclusion may apply to the solving of mazes, which
younger chimpanzees can plan out to two steps (Völter & Call, 2014). Some notion of
causality must be present, as the animal must understand that the solution of one step affects
the next. However, this does not detract from the general conclusion that their causal
understanding is limited.
It is not clear that area 10 supports causal understanding, so much as it supports the
comparison of the current and end states of a problem in working memory, an evaluation of
the discrepancy, and any task switching needed to reach a solution. There is, however,
another brain area that seems more clearly related to the understanding of causality. In
humans, but not in macaques, a portion of the inferior parietal lobe becomes active in the left
hemisphere during the observation of tool use. More importantly, its activity is contingent on
understanding the goal of using the tool. For example, the area is activated when participants
view a small rake dragging an object, but not when they view the rake moving alone without
an object. Thus, the area, more specifically the anterior portion of the supramarginal gyrus
(Brodmann area 40, see Figure 10.4), appears to grasp causal relations between the intended
use of the tool and the results of using it (Peeters et al., 2009).
Furthermore, tasks requiring the understanding of spatial causality without the use of tools,
such as deciding whether a ball striking another caused it to move, activate the supramarginal
gyrus on the right side (Straube & Chatterjee, 2010; Wende et al., 2013). Thus, the gyrus
seems generally involved in understanding physical causality, with its left-versus-right
manifestation depending on specific aspects of the task.
An understanding of causality is important to planning because it produces solutions when
simple heuristics fail. Thus, we have no difficulty solving the rake-and-pit problem failed by
chimpanzees, because we understand that dragging the rake straight toward us will cause the
food to fall into the pit, and that moving the rake sideways at the right place will avoid that.
Understanding causal relations is one of the things allowing us to innovate when solving
problems.
The fact that humans, but not macaques, have the localized parietal lobe mechanism for
understanding physical causality, dovetails with the observation that beginning with the
genus Homo about 2.4 million years ago, inferior parietal cortex visibly acquired new gyri.
They were specifically the supramarginal gyrus and the angular gyrus, Brodmann areas
40 and 39 (Glover, 2004; Tobias, 1995). It appears, therefore, that humans acquired a new
brain area to allow a deeper appreciation of physical causal relationships. Together with the
planning functions of area 10, these changes helped launch us on the pathway to ever more
sophisticated technologies.
Conclusion
Apes and some monkeys show remarkably diverse tool manufacture and use, which can take
on a cultural dimension and show evidence of diffusion across neighboring communities.
Social learning is the likely mechanism of diffusion, with innovations often introduced by
younger animals. However, most copying of behavior proceeds either peer-to-peer or from
older to younger individuals. In apes, social learning is aided by an ability to understand
requests to “do this”. Actual teaching behaviors are observed for complex skills like nut
cracking, but simpler tasks may involve repeated reinvention instead of teaching.
Across primate species, there is some indication of a positive relationship between
encephalization and the ability to use tools. Thus, primate tool use appears to be both
phylogenetic and cultural in nature.
While precision grip is more widespread among species than was previously appreciated,
humans unlike other apes have a truly opposable thumb that can make pad-to-pad contact
with the index finger. The relatively long thumbs that are possibly a precondition for this,
may date back as far as our common ancestor with gorillas 10 million years ago.
Compared to other primates, humans have evolved both greater hand dexterity and more
forceful grips. Specific evolutionary acquisitions include a hand more capable of cupping
various shapes of objects, a longer thumb relative to the fingers, a more hinge-like thumb
joint, tip-stabilized finger pads that are otherwise mobile, and a horseshoe-shaped crest in the
distal thumb that increases its gripping power.
The result, in part attributable to such influences, was the emergence of worked stone
tools by 3.3 million years ago, developing out of what was presumably an earlier vegetation-
and hammer-and-anvil-based tool tradition. Their maker was probably either Australopithecus
afarensis or Kenyanthropus platyops. In contrast Australopithecus garhi may have manufactured
the tools found at Gona, Ethiopia, dating from 2.6 million years ago.
It seems likely that the biggest factors in the emergence of worked stone tools were
cognitive in nature. Stone tool design progressed from the relatively crude Lomekwian
and Oldowan styles to the highly symmetrical and heavily flaked Acheulean style about
1.8 million years ago. Some later Acheulean tools were made of bone, and include a
barbed hunting point over 700,000 years old. Composite tools adopting other materials
are first known to have appeared about 500,000 years ago, and by about 45,000 years ago
incorporated a variety of forms and materials.
The mental model of a stone tool requires a high degree of three-dimensional spatial
processing, and achieving a satisfactory product requires a mental script including planning
and plan revision. Although apes follow scripts in their tool manufacture and use, human
scripts are more complex, involve more spatial planning, and are more likely to defer success
or failure into the future. Here there appears to be a strong influence of encephalization, with
nearly the same EQ achieved by the likely makers of Lomekwian tools and by the floresiensis
toolmakers on the island of Flores. The relative preservation of Brodmann area 10 in the
dwarfed brain of the latter likely reflects its importance in planning, through its evaluation of
the contents of working memory and its roles in task switching, evaluation of alternative
goals, and allocation of cognitive resources.
In summary, then, it appears that tool use and manufacture on the one hand, and cognitive
evolution on the other hand, have long had intertwined histories. Primate tool use may
depend in part on reaching macaque or capuchin levels of encephalization. However,
changes of brain function and associated structure, and not just size, are likely to have been
equally important. In humans, the development of brain areas such as prefrontal cortex and
the supramarginal gyrus was probably key. The latter in particular seems to be involved in
comprehending physical causality. It and neighboring areas in the inferior parietal lobe
became visible in the human brain beginning with the genus Homo, presumably aiding in
the manufacture of increasingly sophisticated tools.
12 Spatial perception
When an early Euglena-like organism first chased the sun by altering movement of its
flagellum in response to the shading of a photoreceptor, a long evolution of spatial be-
havior was begun. Today, our capacities to identify the location, depth, motion, and
quantity of objects represent some of our most important perceptual abilities. The result
is that we can successfully navigate an environment much more complex than anything
encountered by Euglena.
In this chapter we examine several kinds of spatial information, consider how it is pro-
cessed by complex organisms with emphasis on humans and other primates, and trace
evolutionary changes as far back as data permit us.
Location
The first kind of spatial information is location. Early on, it was sensed using the simple
optical properties of the eye. Thus, a lensless pit eye was capable of determining the general
direction of light through the alignment of photoreceptors with both the light source and the
eye’s aperture (see Figure 7.2). As the pit deepened and the aperture shrunk, approximating a
pinhole eye, localization became more precise because of a substantially improved image
on the retina. Finally, in the lensed eye there was a sharply imaged, one-to-one mapping of
source points to retinal points. Thus, in a straightforward evolutionary sequence, successive
improvements in the structure and physics of the eye led to a more finely tuned ability to
locate a light source.
Of course the eye tells only part of the story, and we must look to its projections to
the brain and the brain itself to complete it. In the human eye, the output of some
130 million receptors are funneled to the brain over 1.2 million optic nerve axons, an
average compression ratio of over 100:1. As we have seen, much of the compression is
accomplished by compromising peripheral vision. Thus, massive numbers of receptors
in the periphery funnel down to relatively few ganglion cells, producing substantial in-
formation compression but poor acuity. In comparison there is little funneling from
receptors in the fovea to a relatively large number of ganglion cells, producing little
compression and high acuity.
These patterns are repeated at V1, the primary visual cortex, where a cortical magnification
factor is apparent. This is a mathematical relationship between the acuteness of an area of
vision and the amount of cortex serving it, so that more cortex is devoted to sharper areas of
vision. As a result much larger numbers of cortical neurons are devoted to an area of the fovea
than to a same-size area of peripheral vision (Born, Trott, & Hartmann, 2015).
In turn, acuity determines the precision of spatial localization. This can be measured by
Vernier acuity, the ability to detect whether two line segments are continuations of the same
line or rather are offset from one another. Vernier acuity is much worse in the periphery than
DOI: 10.4324/9781003137863-15
Spatial perception 207
in central vision. An impression of this can be gained by averting central vision away from the
lines in Figure 12.1, which makes detection of the offset much more difficult. Thus, the
ability to spatially localize the lines is positively related to the degree of cortical magnification
for their location on the retina (Greenwood, Szinte, Sayim, & Cavanagh, 2017).
Figure 12.1 Demonstration of Vernier acuity. The left lines are aligned, while the right ones are slightly offset.
Relative acuity across primate species is fairly well understood, using a version of Vernier
acuity in which two lines are perceived if the gap is discriminable but one line if not.
Measured in that way, acuity in apes (including man) and macaques is nearly twice as good as
it is in strepsirrhines and New World monkeys (Ross, 2000).
Evolutionarily speaking, what happened is that in diurnal anthropoids – including apes,
humans, and macaques – the cornea and lens became reduced in size relative to the rest of the
eye. That allowed their positioning further from the retina, increasing the focal length
(the distance required for an image to come to a focus). In turn that magnified the image on
the retina (Ross & Kirk, 2007). The more magnification, the greater the acuity, because any
given part of the image was spread over more receptors. Night vision degraded, however,
because smaller corneas and lenses meant less light-gathering power. But in diurnal an-
thropoids that did not pose a significant problem, because life’s critical activities were per-
formed in daylight (Ross & Kirk, 2007). These changes to the cornea and lens must have
taken place close to the origin of anthropoids 66 million years ago.
Higher brain mechanisms for recognizing location

So far we’ve really only considered how the appropriate conditions were created for the brain
to recognize location. Although V1 maintains a direct correspondence between a source’s
position on the retina and the location of cortical activation, further processing is needed to
locate the source relative to the self or to the environment.
The brain region most involved in referencing locations to the self is the parietal lobe, the
upper rear portion of the brain. It receives input from V1 partly by way of the immediately
adjacent area V2 (Brodmann area 18, see Figure 10.4), along what is called the dorsal visual
stream. The dorsal stream is sometimes referred to as the “where” pathway to emphasize
its role in spatial processing (Figure 12.2).
Judgment of location relative to the body uses what is called the egocentric frame of reference.
Deciding whether an object is to the left or right of our position, and to what degree, refers
to ourselves and is therefore ego-oriented. For example, Neggers and colleagues asked
participants to judge the position of a vertical bar superimposed on a horizontal bar, in
Figure 12.2 The dorsal and ventral visual streams.

Source: 1424 Visual Streams.jpg, CC BY-SA 3.0, OpenStax College.
relation to the middle of the body. Activation was found in the superior parietal lobe,
Brodmann areas 5 and 7. This activation was not found when the positions were judged in
relation to the center of the horizontal bar, an environmentally-referenced judgment using
what is called the allocentric frame of reference. That uses the ventral visual stream of processing,
located in the temporal lobe (Figure 12.2; Neggers, Van der Lubbe, Ramsey, & Postma,
2006), including the hippocampus (Box 12.1).
Box 12.1 Place cells, grid cells, and the hippocampus.
Located in the medial temporal lobe, the hippocampus is a ridge of gray matter
roughly in the shape of a sea horse: Thus, its name, which is Latin for sea horse. It
makes up part of the ventral stream of processing, and is the site of place cells, neurons
that respond to particular locations in the environment. Place cells in turn connect to
grid cells, neurons that respond to locations in an overall grid representation of the
environment. Because the representation is environmental – the grid is in effect a
map – it is allocentric. Grid cells can be found both in the hippocampus and in
neighboring cortex ( Jacobs et al., 2013).
Both place and grid cells have been found in humans undergoing electrode
placements in their brains to locate the source of epilepsy prior to possible surgical
treatment ( Ekstrom et al., 2003; Jacobs et al., 2013). They have also been found in
rhesus macaques ( Killian, Jutras, & Buffalo, 2012), rats and mice ( Fyhn, Hafting,
Witter, Moser, & Moser, 2008), and bats ( Yartsev, Witter, & Ulanovsky, 2011).
Furthermore the grid cells of bats are very similar to those of rats, e.g., in grid layout,
cell layering, and the correlation of cell firing with movement velocity ( Yartsev et al.,
2011). That suggests that they, and presumably place cells as well, have a very long
evolutionary history dating back beyond the last common ancestor of bats, rats, and
humans – which lived a bit in excess of 80 million years ago ( Springer et al. 2017;
Tarver et al., 2016).
There is evidence that the size of the hippocampus is related to how much it is used
in spatial processing of the environment. Birds that cache food for later retrieval, such
as the marsh tit and black-capped chickadee, have larger hippocampi than related
species that do not cache food (for the examples given, the bridled titmouse and the
Mexican chickadee). Similar results apply in rodents ( Roth, Brodin, Smulders,
LaDage, & Pravosudov, 2010). They have even been found in humans: University
students who better learned a mental map of campus, as evidenced in a task requiring
them to point to relative locations while blindfolded, had larger posterior hippocampi
than those who performed more poorly ( Schinazi, Nardi, Newcombe, Shipley, &
Epstein, 2013). This confirmed other studies examining navigation in taxi drivers
( Woollett & Maguire, 2011).
Other studies indicate that the area of activation involved in egocentric location judgments
may be narrowed down to area 7 and the bordering posterior intraparietal sulcus (Zaehle
et al., 2007). Furthermore, when hemispheric differences are found, the right hemisphere is
more involved than the left (Iachini, Ruggiero, Conson, & Trojano, 2009). Right hemi-
sphere lateralization is also evident in visual field studies, in which a dot is presented in the
left or right visual field and the task requires subsequent report of the location. Accuracy is
generally higher in the left visual field, projecting to the right hemisphere (Boles, Barth, &
Merrill, 2008).
It is no accident that egocentric location processing emphasizes the dorsal pathway and the
parietal lobe, while allocentric processing emphasizes the ventral pathway and the temporal
lobe. Recall that the parietal lobe is also the principal location of somesthetic processing.
In representing the body’s surface, SI is highly egocentric. Thus, evolution appears to have
unified egocentric representation by placing the tactile and visual frames of reference in
proximity within the same lobe. Indeed, in the macaque many neurons in the superior
parietal lobe respond to both visual and somesthetic stimulation (Gamberini et al., 2018;
Gamberini, Galletti, Bosco, Breveglieri, & Fattori, 2011). In contrast, allocentric location
processing depends heavily on referencing objects in the environment. As we shall see in
the next chapter, object recognition is largely performed in the temporal lobe as part of the
“what” pathway (Figure 12.2).
In the macaque, the intraparietal sulcus (Figure 12.3) has neurons that code the coordinates
of visual stimuli in a head-centered, egocentric frame of reference. There is substantial
sensitivity of the sulcus to motion of both the stimulus and the body, providing spatial
updating that prepares the animal for movement (Grefkes & Fink, 2005).
The use of area 7 and the intraparietal sulcus for egocentric processing may trace to early
primates. Galagos, which are strepsirrhines, have a large posterior parietal area, while our
close nonprimate relatives the tree shrews do not (Kaas, 2013). However, egocentric
processing is performed by species as diverse as mice, birds, and insects (Benhamou &
Poucet, 1996; Bruck, Allen, Brass, Horn, & Campbell, 2017), presumably using other
neural mechanisms.
Depth
Other processes are devoted to localization in a dimension not yet considered, the one in-
volving positions nearer to or farther from the observer. Depth can be computed from many
cues, but four are particularly powerful. Three are monocular cues because they can be seen
by a single eye, as opposed to the fourth, which is a binocular cue (requiring two eyes to see).
The monocular cues are occlusion, in which an object whose image partially blocks another
is judged closer; relative size, in which the images of two similar objects are compared and the
1,2,3 7
intraparietal sulcus
inferior parietal lobe
40 39
43
Figure 12.3 Major features of the parietal lobe, referenced to numbered Brodmann areas.
Source: Adaptation of Gray726-Brodman.svg, public domain, Henry Vandyke Carter and Tkgd2007.
larger is judged closer; and height in the visual field, in which the images of objects lower in the
visual field are usually judged closer than those higher in the visual field (Glueck, Crane,
Anderson, Rutnik, & Khan, 2009). All emerge from location processing, as well as more
general pattern recognition processes covered in the next chapter.
Here, attention focuses on the binocular cue specifically. It is called binocular disparity,
the discrepancy between images from the two eyes. In order to compare images across eyes
for the purpose of detecting disparities, it is necessary for them to come together in the
primary visual cortex (V1). As we have seen, after the optic nerves leave the eyes, they split
with the inner halves crossing over and the outer ones passing straight back (Figure 7.6). As
a result the inner half of the one eye and the outer half of the other eye, both surveilling
the same visual field, project to the same hemisphere of the brain. The outputs from their
images come together and are compared in V1, which has cells that directly detect bi-
nocular disparity.
Across species, the use of binocular disparity as a depth cue depends heavily on the spatial
arrangement of the eyes. A minimal requirement is that the eyes be capable of imaging the
same object at the same time, achieving binocular convergence. This is not as trivial as it seems
since many species (e.g., horses) have eyes located on the sides of the head nearly opposite
one another. Because such species have only a small overlap between what the two eyes see,
binocular disparity cannot be used as a depth cue in most of the visual field. Other species,
however, including primates, have their eyes shifted forward so they face the same direction.
Images with much greater overlap are produced, providing disparity cues throughout the
visual field.
Binocular vision has a deep history within primate ancestry. Even the earliest primates
showed substantial binocular convergence. Convergence can be measured as the binocular field
of view (BFOV), i.e., the opening angle of the joint field of view. If you close your left eye
and look straight ahead, you can move a fingertip left until it disappears behind your nose
about 70° left of center. If you repeat the process with the right eye, the fingertip disappears
about 70° right of center. Both eyes can see everything within those limits, a joint field of
view of about 140°.
Rats at 40–60° and tree shrews (close relatives of primates) at 60° have BFOVs less than
half that amount. In contrast the early Eocene primate species, Teilhardina asiatica, dating to
55 million years ago, had an estimated BFOV of about 110–120°. That value is not much less
than the 127–128° value of tarsiers, the 135° value of galagos, the 138–146° values of New
World owl and squirrel monkeys, and even the 140° to 160° values of macaques and modern
humans (Heesy, 2004; Ross, 2000).
Thus, binocular convergence was largely in place during an early phase of primate evo-
lution, increasing only modestly during our descent. It testifies to an origin in nocturnal
predation, as it is believed to have been used by early primates to counter camouflage by
detecting depth disparities between an insect and its surroundings (Heesy, 2008; Ni, Wang,
Hu, & Li, 2004). In fact predators in general, not just primates, tend to have front-facing
vision, because the overlap between the eyes provides good depth perception to discern and
attack prey. In contrast prey animals tend to have side-facing vision with little binocular
overlap, for maximal surveillance of the environment.
Another factor is that larger bodies have greater separation between the eyes, increasing
disparity cues and improving depth perception. In fact in our ancestral line, eye separation
increased dramatically as body sizes increased. Thus, Teilhardina asiatica weighed only about
1 ounce and had an inner interorbital distance (the space between the eyes, as measured
between their nearest edges inside the skull) measuring only 4 mm (Ni et al., 2004). In
contrast the typical interorbital distance in modern humans is on the order of 20–30 mm
(Mafee et al., 1986).
Figure 12.4 A random-dot stereogram. Slightly crossing the eyes so that the squares lay atop one another and
fuse, produces a perception of abstract shapes in depth.
Source: Adaptation of Stereogram Tut Random Dot Shark.png, CC BY-SA 3.0, Fred Hsu.
Depth perception, however, requires further cortical processing beyond mere con-
vergence between the eyes in V1. Tsao and colleagues (2003) used random-dot stereograms
(simpler but otherwise similar in structure to Figure 12.4) to examine brain mechanisms of
depth perception in both humans and macaques. Binocular fusion of two stereogram views
resulted either in a perception of depth or of no depth. When depth was present, there were
widespread increases in cortical activation that were strongest in both species in area V3a and
the caudal (rear) intraparietal sulcus (Tsao et al., 2003). Area V3a is in the occipital lobe
bordering on the parietal lobe, and like the intraparietal sulcus is thus part of the dorsal
“where” stream of processing.
However, to some extent depth is also processed along the ventral “what” pathway (see
Figure 12.2; Georgieva, Peeters, Kolster, Todd, & Orban, 2009). There it is used to re-
cognize objects in depth rather than their location as such (Verhoef, Vogels, & Janssen,
2016). Perceiving 3D shapes uses this pathway.
Motion
Other cues for perceiving depth come from motion. If one object moves to occlude another,
partially or completely hiding it, then the occluding object is presumed to be closer to the
observer. More subtly, as we move toward objects, ones that are closer show substantial
moment-to-moment change in the size and position of their image at the retina, while those
farther away show relatively little change. Vehicle occupants notice this in the form of optic
flow, the experience of objects rushing past in the periphery while the view of the road far
ahead seems to change much more slowly. However, optic flow is more than just a depth
cue, because it also provides essential information as to heading, i.e., the direction of
movement. Given stationary objects, eyes, and head, the point in space from which flow
seems to emanate is the direction in which the observer is moving.
Both monkeys and humans use optic flow, and show at least somewhat similar patterns of
cerebral activation. In humans, studies using two different brain imaging technologies, po-
sitron emission tomography (PET) and functional magnetic resonance imaging (fMRI; for both, see
Box 12.2) found that human observers passively viewing optic flow showed activation in area
MT/V5 (see Figure 13.1), located in part of the inferior temporal sulcus (Sunaert, Van
Hecke, Marchal, & Orban, 1999). The same was found during the active determination of
heading, although parietal activation was also observed (Peuskens, Sunaert, Dupont, Van
Hecke, & Orban, 2001). These results indicate that MT/V5 is sensitive to the movement
present in optic flow, while the parietal lobe performs the spatial computations needed to
determine heading.
Box 12.2 PET and fMRI imaging.
Positron emission tomography, or PET, involves injecting a radioactive substance into

the bloodstream, either intravenously (e.g., radioactive glucose) or via respiration (e.g.,
radioactive oxygen). For safety reasons, substances with short half-lives are used to limit
the amount of radiation emitted.
When brain areas are active due to the performance of a task, blood flow increases
locally, perfusing the tissue with the radioactive substance. As radioactive decay occurs,
positrons are emitted. Each positron is annihilated on contact with an electron,
emitting a pair of photons with each pair member at a 180° angle to the other. An
apparatus outside the head detects these pairs, and computer calculations work out their
point of origin. As a result, over a short period of time enough pairs are detected that
an image can be constructed of activity in the brain. However, this method does not
produce a physical image of the brain on which the activation image can be
superimposed. Instead activation is usually specified in Talairach space, a set of X, Y,
and Z coordinates that relate it to structures in an “average” brain.
Functional magnetic resonance imaging, or fMRI, provides more precise localiza-
tion of function by overlaying an image of brain activity on an image of the physical
brain. It works by first using an intense magnetic field to induce spinning protons in
some of the brain’s hydrogen atoms to align with lines of force. This is followed by a
radio frequency pulse that deflects the protons, causing a wobbling of their spins.
Detectors of electrical currents outside the head time the realignment of protons with
the magnetic field once the radio pulse is turned off. As it happens, this timing is
affected by whether the protons are in gray matter or white matter, allowing
construction of a physical image of the brain. It is also affected by the level of blood
oxygenation, indicating which brain areas have been more active. The resulting
functional image can then be overlaid on the physical image, allowing activation to be
localized precisely in relation to brain structures.
For their part, macaques have an equivalent of human area MT/V5 that is sensitive to
motion. It responds most to coherent motion in one direction, although incoherent motion
provokes a response of lesser degree (Zaksas & Pasternak, 2005). Comparative studies suggest
that this area exists in all primates including galagos, but not in species related to primates
such as tree shrews. It therefore appears to have been a primate innovation (Kaas, 2004b).
However, the ventral parietal cortex of monkeys is also involved in perceiving optic flow,
with most neurons responding to expansion but some to contraction (Bremmer, 2005). This
area may differ somewhat from that used by humans to perceive heading, which is more
dorsal than ventral in location (Peuskens et al., 2001).
Quantity
The ability to judge quantities has clear adaptive value, for it can help determine which tree
has more fruit, or which way to run when escaping groups of predators. In the absence of
verbal counting, which is presumably a recent addition to hominin capabilities, quantity
perception must rely on some type of spatial representation.
Studies of quantification in modern humans indicate the existence of three separate
processes. When varying numbers of stimuli such as dots are presented briefly, and observers
are asked to specify their number as quickly as possible, a three-limbed function is produced
relating reaction time (RT) to numerosity (Figure 12.5). The first limb is from 1 to 3 or
4 dots, showing a modest increase in RT with each additional dot. The second is from
3 or 4 to about 7 dots, with a steep increase per dot. Finally, the third limb is marked by
negligible increases in RT from about 7 dots on.
There has been little controversy over the nature of the second and third limbs. The
second has been held to be due to an explicit counting process that involves verbalization and
working memory, two time-intensive components that account for the substantial increase in
RT as the number of dots increases. The third limb is due to an estimation process that kicks
in when the number of dots is too large to be counted within the brief memory of the
display. In fact when the display is left on until response, RTs continue to rise with an
increasing number of dots – i.e., estimation does not occur – because counting continues to
completion. Because brief display of a large number of dots involves a single numerical
estimation, RT is not much affected by the number of dots (Mandler & Shebo, 1982).
Subitizing in humans
Greater controversy has surrounded the first limb of the numerosity curve. Although held by
consensus to reflect a subitizing process (an early perceptual process that rapidly enumerates
small numbers of items), attempts to further characterize it have ranged widely. They have
Figure 12.5 The numerosity curve, relating the number of dot stimuli to the time required to enumerate
them.
included explanations based on the large proportional differences that exist among small
numbers, making them more discriminable than differences among large numbers (Averbach,
1963); the ability of small numbers of items to form patterns such as triangles and lines
(Mandler & Shebo, 1982); a “fast counting” process specific to small numbers (Gallistel &
Gelman, 1992); and a preattentive tagging of item locations that is limited in capacity and
therefore specific to small numbers (Trick & Pylyshyn, 1993).
However, more recent research strongly supports the “fast counting” interpretation of
subitizing (Boles, Phillips, & Givens, 2007). The research was motivated by the observation
that extracting number information from a specific type of bargraph involves the same
perceptual process as extracting number from dot clusters (Figure 12.6). Thus, both are better
recognized in the left visual field (LVF) as opposed to the right visual field (RVF), indicating
a right hemisphere processing advantage. Significantly, the visual field differences are cor-
related so that observers with a large LVF advantage on one also tend to show a large LVF
advantage on the other (Boles, 1991). Furthermore, trainees who practice bargraphs show
substantial transfer of training to dot clusters but not to other numerical tasks (Boles, 1997),
and simultaneous performance of the two tasks produces more interference than pairing
either with a different task (Boles & Law, 1998). All of these observations indicate that the
two tasks share a common process.
Figure 12.6 Examples of dot clusters and bargraphs that use the same perceptual process. The horizontal
reference lines for the bargraph are at the 0, 4, and 8 levels, with the example reflecting the
value “2”.
Figure 12.7 RTs to dot clusters and bargraphs in Boles et al. (2007). Closed symbols LVF, open sym-
bols RVF.
Source: Response times from Study 1, reprinted by permission from Springer Nature Customer Service Centre GmbH,
David B. Boles, Jeffrey B. Phillips, Somer M. Givens.
The experiments of Boles et al. (2007) examined the relationship between the tasks in
more detail, beginning with the plotting of numerosity curves. The dot clusters showed
the classic multi-limbed function (Figure 12.7). The bargraphs, in contrast, showed an
intriguing scallop-shaped function in which small increases in RT occurred at values
starting at 0, 4, and 8 – i.e., the values represented by the horizontal reference lines
(Figures 12.6 and 12.7). This pattern of small RT changes with increasing number sug-
gested that the same subitizing process underlies the enumeration of small numbers of dots
and the enumeration of bargraphs. The suggestion was strongly confirmed by other re-
lationships in the results between the bargraphs and the subitizing range (1–4) of dot
clusters that were not found between bargraphs and the higher range (5–8) of dot clusters
(Boles et al., 2007).
The importance of these observations is that by establishing that subitizing underlies
bargraph recognition, the nature of subitizing is revealed by the pattern of bargraph RTs.
The scallop-shaped RT function is a telltale indication that subitizing is a rapid, nonverbal
counting process operating on analog quantities. In the case of bargraphs the analog quantities
are imaginary intervals or steps above or below the reference lines, while in the case of dot
clusters they are the dots themselves. Because subitizing uses analog quantities, it seems
reasonable to classify it as a spatial process. Furthermore, consistent with subitizing’s spatial
nature, brain imaging studies implicate right parietal lobe involvement, involving either the
intraparietal sulcus (Cutini, Scatturin, Moro, & Zorzi, 2014) or area 39 at its junction with
the temporal lobe (He, Zuo, Chen, & Humphrey, 2013).
Subitizing in other primates

Do other primates subitize? The most comparable study is of a chimpanzee named Ai, who
was trained to associate the Arabic numerals 1–7 with the appropriate numbers of dots in a
display, and to press the appropriate numeral (Murofushi, 1997). She was subsequently timed
in her responses to varying numbers of dots. Her results were strikingly similar to those from
human participants. Tested on 1 to 7 dots, a subitizing range of 1 to 3 or 4 dots was clearly
differentiated from a “counting” range of 3 or 4 to 6 dots (Figure 12.8).
Figure 12.8 Numerosity curves for a chimpanzee responding to 1–7 dots. RT = Reaction time.
The results indicate that chimpanzees likely engage in the same analog-based subitizing
process as humans. What they do in the “counting” range is less clear since they presumably
do not have the same verbal processes as humans. Murofushi observed that with the larger
numbers Ai’s eyes tended to move back and forth between the display and the response
numerals, as if taking additional decision time – a possible cautionary note for research on
human enumeration in suggesting that large increases in RT can in fact be due to processes
other than verbal counting.
There are indications that macaques show much the same behavioral pattern of results
when enumerating items, as well as at least some parietal lobe involvement. Nieder,
Freedman, and Miller (2002) used a somewhat different experimental design requiring rhesus
monkeys to compare quantities of successive patterns of 1–5 dots. The resulting numerosity
curve nevertheless showed a strong resemblance to that found for humans and chimpanzees,
except that the subitizing range was limited to 1 to 2 dots rather than 1 to 3 or 4 dots (Nieder
et al., 2002.)
Nieder et al. also recorded from single neurons in monkeys performing the task, and
found that 7% of inferior parietal cells, and about a third of randomly selected prefrontal
cells, showed activation that varied with the number of dots. Furthermore, individual
neurons were “tuned” to a particular number, so that some responded with peak activity
to one dot, others to two dots, and so on, indicating an individual-neuron based sensitivity
to numerosity. The involvement of inferior parietal cells is generally consistent with the
human literature cited earlier.
Because there is at least some inferior parietal involvement in subitizing in macaques, it
appears that use of the area for that purpose traces back at least to the origin of Old World
monkeys about 29 million years ago. Thus, basic numerical ability far predates the symbolic
representation of number in hominin artifacts (Box 12.3).
Box 12.3 Quantity representation in hominin artifacts.
Numerous examples have been discovered of hominin artifacts of relatively late date
that may – or may not – symbolize quantity. Specifically, bones bearing roughly
parallel cut marks have been found, most dating to 10,000–42,000 years ago but some
earlier. The challenge lies in distinguishing markings used as symbolic quantities, from
those merely appealing to a sense of aesthetics ( d’Errico et al., 2018). Thus, a row of
vertical marks on a bone might represent a kind of tally, or it might just be a pleasing
pattern (see Figure 12.9).
Figure 12.9 A bone artifact displaying five cut marks of ambiguous significance.
Source: Detail of cut marks (FindID 96513).jpg, CC BY-SA 4.0, The Portable Antiquities Scheme/The Trustees of the
British Museum.
D’Errico and colleagues have suggested clever criteria to distinguish between the
possibilities. An aesthetic artifact might be expected to have equidistant markings, and
might be embedded in a larger pattern. A symbolic use of cut marks, in contrast, would
not be embedded, and the marks would not be equidistant because its maker would be
interested only in the tally, not in the spatial precision of the marks. By these criteria,
the artifact in Figure 12.9 might be interpreted as a tally. Judging from the oldest
examples, a shift from exclusively aesthetic uses of cut marks to more symbolic ones
may have occurred by 60,000 years ago ( d’Errico et al., 2018). This, of course, long
postdates the acquisition of basic numerical abilities in our ancestral line – but it long
predates the development of mathematics.
How much further than 29 million years ago it extends is presently unclear. Like primates,
crows have neurons sensitive to number, but it is uncertain whether that is due to convergent
evolution, or to shared ancestry dating to over 300 million years ago (Wagener, Loconsole,
Ditz, & Nieder, 2018).
Orienting
Spatial perception is enhanced by our ability to shift eyes and attention toward a source of
stimulation, in other words orienting to objects. This allows more precise estimates of location
and depth. The parietal lobe plays a major role in orienting. In humans, both saccades (eye
movements toward a source of stimulation) and pursuit eye movements (eye movements fol-
lowing a moving object) involve an area in the middle of the intraparietal sulcus including a
portion of Brodmann area 7 (Culham, Cavina-Pratesi, & Singhal, 2006; Olson, Gatenby,
Leung, Skudlarski, & Gore, 2003). It is sometimes called the parietal eye field, and one of its roles
is to update spatial information in response to movement (Culham et al., 2006). In addition, it
may actually initiate eye movements (Pierrot-Deseilligny, Ploner, Müri, Gaymard, & Rivaud-
Péchoux, 2002), although others take the position that it maintains eye movement accuracy
(Rafal, 2006). As we have seen, galagos have a large posterior parietal lobe, and so the in-
volvement of the intraparietal sulcus and area 7 may trace back to the early history of primates.
Eye movements also involve a second important area, the frontal eye field, located in the
frontal lobe. There is increasing consensus that it is located near the rear of the middle frontal
gyrus (see Figure 10.3), more specifically at or close to the intersection of the superior frontal
sulcus with the precentral sulcus (Petit & Pouget, 2019; Rafal, 2006). Research suggests it
plays a larger role in triggering voluntary saccades (i.e., to a stimulus long present) than
in triggering reflexive saccades (i.e., to the sudden appearance of a stimulus; Rafal, 2006).
This may be a matter of degree since bilateral lesions of both the frontal and parietal eye fields
appear necessary to cause a severe, long-lasting effect on both voluntary and reflexive sac-
cades (Pierrot-Deseilligny et al., 2002).
Spatial attention, the ability to attend to objects or locations independent of eye position,
involves parietal areas that overlap with those controlling eye movements. For humans,
posterior parietal cortex (Brodmann area 7), was highlighted as critical to spatial attention by
Posner and colleagues (Posner, Walker, Friedrich, & Rafal, 1984). They presented lesion
evidence indicating that the area is involved in the engagement and disengagement of at-
tention to positions in space. The bordering intraparietal sulcus is also activated by the
preparation and movement of attention to the periphery, even if the eyes are kept fixated in a
central location (Astafiev et al., 2003).
A second parietal area involved in spatial attention is the inferior parietal lobe. When it is
damaged, a syndrome called visuospatial neglect (or visual neglect, or spatial neglect) can result.
The patient fails to orient to objects opposite the side of the lesion. The syndrome most often
(but not exclusively) follows right hemisphere damage, thus producing a left-sided neglect.
The symptoms can be quite striking, as when patients draw objects with their left sides
missing, or bisect lines far to the right of their actual midpoints. A companion phenom-
enon, pseudoneglect, can be observed in normal individuals by requiring the bisection of
lines staggered down a page. Bisections are typically made slightly to the left of true center,
opposite to the effect seen in most neglect patients. This result is attributable to an intact
right hemisphere attentional mechanism that overattends to its half of space, resulting
in overestimation of line length on that side (Boles, Adair, & Joubert, 2009; McCourt,
Garlinghouse, & Reuter-Lorenz, 2005).
Several studies have mapped the lesions of patients with visuospatial neglect. Taken
together they find that the critical damage is either in the posterior portion of area 40 or
the adjoining area 39 (e.g., Mort et al., 2003; Ptak & Schnider, 2011; Verdon, Schwartz,
Lovblad, Hauert, & Vuilleumier, 2010). Since both area 40 (the supramarginal gyrus) and
area 39 (the angular gyrus) border on and are inferior to the intraparietal sulcus (see
Figure 12.4), it is an interesting question whether they represent the same or a different
area than that identified in attention shifting. The available evidence suggests that it is
in fact different. Astafiev et al. (2003) found that after accounting for areas involved in
saccades, a small portion of Brodmann area 7 could be attributed to spatial attention
specifically. In contrast, the lesions involved in neglect appear to lie in the ventral portions
of areas 39 and 40 and thus at some remove from area 7 and the intraparietal sulcus.
Therefore areas 40/39 and 7 may well support separate components of spatial attention.
The evolutionary background of orienting

Evidence from primates suggests that the orienting mechanisms found in humans have a long
evolutionary history. In macaques, eye movements involve a lateral intraparietal location
believed to correspond to the human parietal eye field. However, there may be a small
difference in that the area is located in the lateral intraparietal sulcus in monkeys but at its
medial wall in humans. Monkeys also have a frontal eye field, but at a location somewhat
anterior to ours (Astafiev et al., 2003; Culham et al., 2006; Grefkes & Fink, 2005). They
probably derived this from a common ancestor with galagos, for galagos likewise have a
frontal eye field (Stepniewska, Pouget, & Kaas, 2018). Its appearance therefore seems to date
at least as far back as the strepsirrhine divergence 68 million years ago.
Further parallels are found in attention. Just as human attention and eye movements in-
volve similar parts of the intraparietal sulcus, macaque attention and eye movements both
involve the lateral intraparietal sulcus (Astafiev et al., 2003; Grefkes & Fink, 2005). There is
even an indication of a similar mechanism involved in spatial neglect, and in a species with an
older evolutionary divergence from humans. Specifically, in marmosets neglect is produced
by lesions of the parietal lobe, extending down to include part of the temporal lobe. The
affected animals have difficulty locating rewards opposite their lesions (Marshall, Baker, &
Ridley, 2002). While the critical part of the lesioned area producing this behavior is not
known, the result raises the strong possibility that monkeys have equivalents to both of the
attention-related parietal areas found in humans.
Reaching and grasping

Orienting allows us to “home in” on locations and objects, not just as an aid to judging
location and depth, but also for the purposes of reaching and grasping. In both macaques and
humans, the most posterior part of the superior parietal lobe is involved, on its medial surface.
In humans that is the medial part of area 7, known as the precuneus (Gamberini et al., 2018;
Vesia et al., 2017).
Grasping independent of reaching, however, appears to involve the anterior intraparietal
sulcus, and immediately below it, the superior rostral (forward) portion of area 40 (Frey,
Vinton, Norlund, & Grafton, 2005; Vingerhoets, 2014). This introduces an inferior parietal
component to the processing of spatial location, perhaps because grasping is more object-
oriented than the more purely egocentric tasks eliciting superior parietal activation.
The two parietal areas principally involved in recognizing location, areas 7 and 40, both
showed evolutionary change in our immediate ancestry. A bulge of the parietal region,
observed in Homo sapiens, has been attributed to an expansion of the precuneus of area 7. The
bulge, and the expansion, are not observed in chimpanzees. Nor is it evident in Neanderthal
endocasts (Bruner, 2010; Bruner, Preuss, Chen, & Rilling, 2017). For its part, the supra-
marginal gyrus, the location of area 40, is evolutionarily recent and has no analog in ma-
caques. Nevertheless, the anterior infraparietal area is involved in grasping in both humans
and monkeys (Vingerhoets, 2014).
Navigation
As perceptual information is progressively processed in the “where” pathway in the parietal
lobe and then in the frontal lobe, its coding becomes more action-oriented, matching percept
to motion. All of this activity comes together in our ability to navigate our environment.
As we learn to navigate, memory becomes increasingly important. It allows us to recall the
locations of landmarks, and to associate with them actions such as turning left or right.
Generally speaking, when we find ourselves in a new environment, whether it is a new
building or a new city, most of us initially build route knowledge, assembling knowledge of
landmarks and the associated turns to learn pathways from one point to another. As learning
progresses, we gradually develop more sophisticated survey knowledge, which is the knowledge
of how landmarks are configured relative to one another. At this point a true cognitive map
develops, allowing us to deviate from established pathways and find new routes (Wolbers,
Weiller, & Büchel, 2004). However, there are individual differences in the formation of
cognitive maps. Some individuals begin to acquire information about spatial relationships and
start building a cognitive map on first exposure to a new environment, essentially bypassing
the route knowledge phase. Others never proceed beyond route knowledge to build a
cognitive map (Ishikawa & Montello, 2006).
There is good evidence that many chimpanzees develop true cognitive maps. In African
forest habitats they follow nearly linear paths to food trees scattered among many thousands
of other trees, with the vector varying depending on the relative locations of the tree and
themselves. They also decelerate when nearing the goal. The implication is that the
chimpanzees “know” where they are going on a mental map (Normand & Boesch, 2009).
Similar results were found by Janmaat, Ban and Boesch (2013), who followed the foraging
behavior of five female chimpanzees for several weeks. They reported that 13% of close
inspections of food trees were preceded by vector-like goal-directed approaches.
Counterintuitively, the use of linear routes increases when territory is less familiar, perhaps
because the animals minimize travel time through territory shared with other, often
aggressive, groups ( Jang, Boesch, Mundry, Ban, & Janmaat, 2019).
Brain mechanisms in navigation

Not surprisingly, the parietal lobe plays a major role in the acquisition of navigation-relevant
knowledge. Shelton and Gabrieli (2002) created a computer-based virtual convention center, a
market place, and a park, with individual human participants assigned one venue for route
learning and another for survey learning. Route learning used a virtual walk-through of the
venue, while survey learning used an aerial perspective to show multiple landmarks simulta-
neously. Scans of brain activity were made during learning, using fMRI. Greater activity was
found for route learning than for survey learning in portions of bilateral Brodmann areas 5 and
7, and right area 40, all in the parietal lobe. Survey learning produced greater activation than
route learning in another portion of area 7 bilaterally. As might be expected, other areas were
also implicated and were probably related to memory, visual object perception, and movement
components of the complex task.
Wolbers et al. (2004) created a virtual town consisting of buildings and roads, and imaged
brain activity while participants both learned the environment by navigating it, and retrieved
information concerning it. The development of route as opposed to survey knowledge was
encouraged by emphasizing landmarks. It was confirmed by checking maps drawn after the
scans, which showed accurate learning of landmark pairs but poor survey learning. Activity in
inferior locations in both parietal lobes, Brodmann areas 39 and 40, was associated with better
learning. Learning-related activation was also found in the medial frontal gyrus and medial
retrosplenial cortex (cortex immediately posterior to the corpus callosum), perhaps related to
movement and memory respectively (Wolbers et al., 2004).
Another approach to uncovering the brain areas critical to navigation uses correlational
methods to relate activation to navigation performance. Moffat, Elkins, and Resnick (2006)
examined route learning in a virtual building, and found a correlation between navigation
accuracy and activation in parietal area 7. Correlations were also reported for widespread
areas including the cerebellum, inferior and middle frontal gyri, and medial temporal and
cingulate cortex among others.
Together these studies indicate that much of the spatial information used in navigation is
processed by the parietal lobe, involving both posterior and inferior locations. The complex
nature of navigation tasks, however, makes it impossible to ascribe them as a whole to a
particular brain area due to the involvement of other areas in memory, object perception, and
movement, all critical to navigation.
Comparable primate data are limited. However, Sato, Sakata, Tanaka, and Taira (2006)
made recordings from individual neurons in the medial parietal cortex of Japanese ma-
caques, while the animals navigated a virtual building with a joystick, using previously
trained route knowledge. About a third of the neurons were found to be sensitive to
movement in the navigation task, most of them in a highly selective manner (e.g., re-
sponding only to a left turn at a particular point). To confirm these results, an agonist
(a drug that temporarily binds to neural receptors and prevents their normal function) was
next injected at the sites, and navigation was subsequently found to be impaired. Thus,
like humans, monkeys appear to make use of parietal mechanisms during navigation. To
the extent that those mechanisms involve the posterior parietal lobe, especially area 7, they
may have originated early in the primate line.
The independence of spatial processes

Given that the parietal lobe is involved in so many spatial functions, it is tempting to
deemphasize the differences between them and to view the lobe as a general-purpose spatial
processor. By this view it might be regarded as relatively undifferentiated in function, with
perception of location, depth, motion, and quantity of objects, and our ability to orient to
them, merely representing minor variations on an overall theme.
There are good reasons to think otherwise, however. First, as already reviewed, different
abilities draw on different parts of the parietal lobe. That indicates that at least to some
extent, spatial processes are independent of one another. Thus, e.g., area 7 in the superior
parietal lobe processes location in an egocentric frame of reference and is involved in
reaching, but does not seem to be involved in grasping or in subitizing. Inferior parietal
cortex, areas 39 and 40, is involved in grasping and subitizing but not in egocentric lo-
cation or reaching. As another example, the intraparietal sulcus dividing superior and
inferior parietal cortex is involved in a number of functions, but different portions are used
for different things: e.g., the posterior portion for egocentric location and depth, the
middle portion for eye movements, and the anterior portion for grasping. This involve-
ment of different parietal areas in different abilities argues for a differentiated parietal lobe
housing a number of discrete processes.
The independence of spatial processes is also supported by a series of experiments de-
scribed by Boles (2002). These were conducted with the purpose of examining what
relationships, if any, exist between a number of spatial tasks. The tasks included recognizing
the number represented by a bargraph; judging the intensity of facial emotions; recognizing
the location of a flashed dot; bisecting lines; judging whether a line was above or below a
fixated point; estimating large numbers of dots; and judging which bar of a cross lay on top of
the other. The tasks were all administered to a large number of participants, and visual field
differences were assessed. All but one showed an advantage of the right hemisphere over the
left, as evidenced by faster or more accurate responses to the LVF compared to the RVF.
Nevertheless, even though the same hemisphere was involved in nearly all of the tasks, the
correlations among the task measures were all essentially zero! In other words, knowing the
size of a person’s hemispheric advantage for one task did not at all predict its size for any of
the other tasks, constituting strong evidence of the independence of spatial processes (Boles,
2002). Taken together with the evidence of differing localization of spatial processes, this
indicates that the parietal lobe is differentiated, housing numerous discrete spatial processes. It
will no doubt prove challenging to identify all of them and to work out their evolutionary
backgrounds.
Evolution of the parietal lobe
The involvement of the parietal lobe in both humans and monkeys is the common thread
running through most of the spatial perception literature. This section addresses the extent to
which this region of the brain been conserved, and to what extent it has changed during
hominin evolution.
Gross size comparisons between monkey and human parietal cortex are fraught with
difficulty, because not everyone agrees on cross-species anatomical markers that separate
parietal from occipital and temporal cortex (Semendeferi & Damasio, 2000). Nevertheless
there are some indications of a general expansion. Thus, while occipital cortex appears to be
only about half as large in humans as would be extrapolated from primate data for a brain our
size (Deacon, 1992b; de Sousa et al., 2010), parietal and occipital cortex taken together are
very nearly in line with such extrapolations (Semendeferi & Damasio, 2000). The implication
is that while the entire sector has maintained a constant size relative to the rest of the cortex,
the parietal lobe has expanded relative to the occipital lobe (Grefkes & Fink, 2005). A
quantitative analysis of primate and human brains, based on 29 anatomical landmarks, has
pointed to a specific widening of the parietal lobe in the medial-to-lateral direction, in
humans as compared to chimpanzees. Unfortunately the anterior-to-posterior direction
could not be adequately assessed, again because the border between the parietal and occipital
lobes was unclear (Aldridge, 2011).
Indications of the parietal expansion are seen in hominin remains. Endocasts from
Australopithecus afarensis show a more-developed parietal lobe relative to apes as of
3.2–3.5 million years ago. Subsequently there was a parietal widening, particularly in the
inferior parietal lobe, which is visible in Homo habilis endocasts dating to about 1.8 million
years ago (Tobias, 1995).
Bruner (2004) compared three species within the genus Homo: Erectus, neanderthalensis,
and modern sapiens. Endocast measurements indicated that relative to erectus, neandertha-
lensis experienced a general upward expansion of the brain that was not limited to
the parietal area. Sapiens, in contrast, specifically experienced “extreme enlargement of the
parietal contour”, accompanied by an occipital decrease (Bruner, 2004, p. 290). As a result,
the occipital lobe shifted to a position further under the parietal lobe, in effect rotated
underneath by the parietal expansion. Rotating with it was the cerebellum, moving from a
position under the rearmost portion of the occipital lobe to its present position nearly
under the temporal lobe (Bruner, 2004).
Taking all of these observations together, there appears to have been a continuous
expansion of the parietal lobe relative to the rest of the brain, beginning sometime prior
to the earliest australopithecines for which we have endocasts (3.5 million years old),
through to modern sapiens. In the process some areas of the lobe appear to have changed
more than others. In modern humans the inferior parietal area has about twice the
cortical surface area, relative to the rest of the cortex, as it does in macaques (Orban et al.,
2006). Also, as previously noted, beginning with the genus Homo the inferior parietal
cortex acquired new gyri, specifically the supramarginal and angular gyri, Brodmann areas
40 and 39 (Tobias, 1995).
Accompanying the expansion, there has been a “medialization” of some parietal areas
in humans, relative to more lateral positions in macaques (Grefkes & Fink, 2005).
Enlargement of the precuneus (medial area 7) was part of the expansion, and it was ex-
clusive to sapiens and not neanderthalensis (Bruner et al., 2017). Finally, although it is not
known to be directly related to the expansion, there is some indication that modern
humans have a larger number of functionally distinct areas in the intraparietal sulcus than
do macaques (Orban et al., 2006).
Conclusion
Our capacities to identify the location, depth, motion, and quantity of objects, and to orient
to them, are among our most important spatial perception abilities.
Although the optics of the eye itself allow a one-to-one mapping of source points to the
retina, the greater compression of information from the periphery limits acuity and in turn
our ability to locate objects. This is repeated at the cortex, where a given area at the periphery
engages less cortex than the same area in central vision.
Information passing along the dorsal visual stream to the parietal lobe allows the location of
objects in the egocentric frame of reference. In the parietal lobe, Brodmann area 7 and the
bordering posterior intraparietal sulcus, especially in the right hemisphere, are most involved,
bringing the tactile and visual egocentric frames of reference into close proximity. Macaques
likewise use the intraparietal sulcus for egocentric location processing. Because a large pos-
terior parietal lobe exists in galagos but not tree shrews, the use of the region for egocentric
processing may have originated in early primates.
The allocentric frame of processing, in contrast, references locations to the environment. It
uses the ventral stream of processing, especially the hippocampus and neighboring cortex.
Place cells respond to particular locations in the environment, and grid cells to locations in a
grid representation of the environment. These mechanisms date back at least as far as the
common ancestor of bats, rats, and humans a little over 80 million years ago.
Depth processing involves a number of cues, but binocular disparity is one of the most
powerful. Outputs from the two eyes converge in the primary visual cortex (area V1), which
has cells that detect binocular disparity. Forward-facing eyes, found even in early primates,
allow a great deal of overlap in the two images, and are a feature of predators that use depth
perception to discern and attack prey. Body size also has an important effect, with large
bodies having increased eye separation which helps better resolve depth. In the brain beyond
area V1, depth is processed by the superior occipital lobe and the caudal intraparietal sulcus as
part of the dorsal stream.
Motion provides cues about both depth and heading, the latter through optic flow. Area
MT/V5 is sensitive to the movement present in optic flow, but parietal cortex appears to
perform the spatial computations needed to determine heading. Macaques seem to use similar
areas. Comparative research suggests that MT/V5 is a primate innovation, as it does not exist
in tree shrews.
In humans, reaction time reveals that the perception of quantity in brief visual displays
involves three processes: Subitizing, used for 1 to 3 or 4 items; counting, used for 3 or 4 to
7 items; and estimation, used for more than 7 items. Although several different explanations
have been proposed for the fast processing of the subitizing range, research using both dot
and bargraph displays show that both use the same subitizing process. Because quantities are
only implied in the bargraphs in the form of imaginary quantities above or below reference
lines, subitizing must involve the fast counting of analog quantities.
A chimpanzee named Ai has shown a very similar pattern, as have macaques. These
outcomes imply that chimpanzees and macaques share our subitizing and estimation pro-
cesses, and that they have a kind of slow “counting” process probably based on eye
movements. Monkeys use the inferior parietal lobe for these processes, as do humans at least
for subitizing.
The parietal lobe is also involved in integrating spatial analysis into action. The control of
reaching and grasping involves the precuneus (medial area 7), while grasping without
reaching involves the anterior intraparietal sulcus and the superior rostral part of area 40.
Macaques seem to use much the same general areas even though strictly speaking they do not
have an area 40. Relative to monkeys, we have shifted some areas to more medial positions,
and have evolved a bulge of the parietal region that has been attributed to an expansion of
the precuneus.
We also use the parietal lobe in orienting to objects. The parietal eye field, located in the
middle of the intraparietal sulcus and part of area 7, updates spatial information in response to
movement, allowing the accurate targeting of eye movements. Spatial attention, which is
the ability to attend to objects or locations independent of eye position, is controlled by
posterior parietal cortex (area 7), and by the inferior parietal lobe (areas 40 and 39). When the
latter is damaged, spatial neglect can occur, involving the overlooking of objects on one side
(usually the left) of a display.
Macaques similarly use an intraparietal location for controlling eye movements, but more
laterally than the medial location used by humans. Spatial neglect has been observed in
marmosets following lesions that include the inferior parietal lobe, similar to humans.
In most cases, humans learning to navigate a new environment first build route
knowledge from landmarks, and gradually develop more sophisticated survey knowledge
that allows formation of a true cognitive map. Chimpanzees also use cognitive maps when
they follow linear paths to food trees. During route learning in virtual environments,
activation is found in areas 5 and 7 bilaterally, and 40 in the right hemisphere, with one
study finding bilateral activation of both 40 and 39. During survey learning, a different
portion of area 7 bilaterally is used. One study of the use of route knowledge in macaques
found involvement of neurons in the medial parietal cortex.
The tempting view that the parietal lobe is an undifferentiated spatial processor is refuted
by two lines of evidence. First, different areas of the lobe serve different processes. Second,
experiments using a number of spatial tasks show that the extent to which each draw on the
right hemisphere is independent of the others. Thus, the parietal lobe is differentiated and
houses a number of spatial processes, each of which may have a separate evolutionary history.
Finally, there is evidence of a parietal lobe expansion during human evolution, relative
to the remaining cortex. The lobe at least widened, its lengthening being hard to address
due to the lack of agreed-upon landmarks. A well-developed parietal lobe is apparent in
Australopithecus afarensis endocasts from 3.2–3.5 million years ago. Widening of the inferior
parietal lobe is visible in Homo habilis about 1.8 million years ago. Thus, there appears to
have been a continuous expansion of the parietal lobe relative to the rest of the brain,
beginning at least 3.5 million years ago and extending down to modern sapiens. It included
the appearance of new gyri in the inferior parietal lobe beginning with the genus Homo.
The number of functionally distinct areas probably increased relative to macaques, and
some areas shifted to more medial positions in the parietal lobe.
13 Pattern recognition
Throughout our evolutionary history, survival has depended on distinguishing among objects
in the environment, and within the class of objects that are living things, among predators,
prey, and conspecifics (other members of our species). We depend particularly heavily on visual
recognition, which is achieved by a series of processing stages along the ventral “what”
pathways of the brain (Figure 13.1).
In this chapter, we trace the progress of information processing along these pathways,
achieving the recognition of features and contours on the way to developing a re-
presentation of general form, and ultimately of objects and their classification. Similarities
and differences between ourselves and other species are highlighted, allowing inferences
about the evolutionary origins of our pattern recognition processes.
Localized processes
Once visual information enters the cerebral cortex in area V1, it proceeds in “feed forward”
fashion through a series of locations in the occipital and temporal lobes. However, anatomical
studies indicate that every such location is directly linked to most others (Kolb & Whishaw,
2009), resulting in connections that are partially serial (e.g., V1 to V2 to VP to V4, as
suggested by Figure 13.1) but are also often capable of bypassing intermediate levels (e.g., V1
directly to V4).
Nevertheless the system has a “stages of processing” aspect to it. Single-cell recordings
reveal that information arriving at V1 in the macaque produces activity serially in V2, V4,
posterior inferotemporal cortex (in humans, located just anterior to LO in Figure 13.1), and
anterior inferotemporal cortex (just forward of that), in phases each about 10 msec apart.
About 20 msec after that, prefrontal cortex activates (Thorpe & Fabre-Thorpe, 2001).
Humans show similar “feed forward” processing, although the timing differs (Isik, Meyers,
Leibo, & Poggio, 2014).
All eutherians have multiple visual areas in the cortex, with the number and arrangement
differing dramatically across species. Hedgehogs, with low reliance on vision, have only two
or three (Rosa & Krubitzer, 1999). Galagos have six (Wong & Kaas, 2010), while cats and
apes, both highly visual, have 20 to 30 or more (Rosa & Krubitzer, 1999). In the case of
humans, the locations shown in Figure 13.1 are only the initial ones in a larger network
of visual areas.
There is strong evidence that in the early stages of cortical processing, primate neurons
respond to features of a visual stimulus. These could be a particular line slant or color
at a specific location. At later stages, neurons respond to specific configurations such as a
particular face or object.
DOI: 10.4324/9781003137863-16
Pattern recognition 227
Figure 13.1 Major visual areas in the “what” pathway of the posterior lateral surface of the brain. Some
extend to the medial surface as well.
Source: Adaptation of Human-brain.SVG, CC BY-SA 3.0, Hugh Guiney.
Features and contours

The initial cortical site of feature processing, V1, is also known as Brodmann area 17, striate
cortex, and primary visual cortex. Its neurons are sensitive to line orientations located at
specific retinal positions. They therefore perform a feature analysis by representing a scene
in terms of small segments of contours (Pasupathy & Connor, 2002).
These simple cells are the first in a cascade of feature detectors that starts in V1 (but
see Box 13.1). Complex cells, mostly found in V2, combine the outputs of multiple
simple cells, and thus respond to orientation over a larger area and to movement in
a particular direction. Through further integration of outputs, many hypercomplex cells
respond to edges that have both an orientation and an end. Some cells in V1 and V2
also respond to curvature, color, and luminance (Nunez, Shapley, & Gordon, 2018;
Spillmann, 2014).
Box 13.1 Feature analysis or spatial frequency analysis?
David Hubel and Torsten Wiesel won a Nobel Prize in 1981 for their investigations
of visual information processing. Recording from the visual cortex of cats and
monkeys, they reported feature detection by simple cells. Specifically, the cells
were found to respond to an edge or bar stimulus at a particular orientation at a
particular point in space. They also discovered complex and hypercomplex cells
( Spillmann, 2014).
However, in subsequent years a competing view has strongly emerged. This view
maintains that the cells involved in early stages of visual pattern recognition can better
be characterized as spatial frequency detectors than as feature detectors. The optimal
stimulus for such detectors is a repeating sine wave pattern at a particular orientation – a
grating, not a bar ( Figure 13.2).
Figure 13.2 A spatial frequency stimulus (grating), representing a sine wave pattern at a particular
orientation. The frequency is specified by the number of repetitions per degree of
visual angle.
Source: Sine pattern.png, CC BY-SA 3.0, Setreset.
The spatial frequency model of visual information processing has enjoyed

tremendous success, with many experimentally validated implications that go well
beyond what is possible to describe here ( De Valois & De Valois, 1990). One basic
confirmation is that many visual cortex cells that respond strongly to bars, respond even
more strongly to gratings ( Albrecht, De Valois, & Thorell, 1980).
Nevertheless there is good evidence that people really do detect features. For
example, the time to determine whether two patterns are the same or not is affected
by the number of features they share ( Bagnara, Boles, Simion, & Umiltà, 1982). If
letter patterns are artificially stabilized on the retina, their features – mostly lines and
curves – perceptually disappear and reappear over time ( Topolski & Inhoff, 1995).
Features also sometimes “migrate” from one object to another. Thus, a red “O” and
green “B”, flashed either at the same place with a brief delay, or in different places
simultaneously, might on occasion be perceived as a green “O” and a red “B” ( Botella,
Privado, de Liaño, & Suero, 2011; Prinzmetal, 1981).
The apparent answer to the feature versus spatial frequency puzzle has two parts.
First, about 5% of cells in V1 show larger bar than grating responses ( Albrecht et al.,
1980). This raises the possibility if not probability that there are V1 edge detectors that
exist outside the spatial frequency domain.
The second part of the answer is that by responding to a bar, even if the response
is less than to a grating, spatial-frequency-sensitive cells are nevertheless sensitive to an
edge feature ( Pasupathy, Kim, & Popovkina, 2019). From their output, and from the
output of the other cells responding more specifically to features, more complex
representations can be developed. As information passes through the ventral “what”
system, there is increasing sensitivity to contours and colored abstract shapes
( Pasupathy & Connor, 2002; Pasupathy et al., 2019). Thus, both spatial frequency
analysis and feature analysis have roles in play in any full account of the early stages of
visual pattern recognition.
Clearly a wide range of information is coded by V1 and V2 cells: Orientation, movement,
curvature, color, luminance, and spatial frequency (Box 13.1) at a minimum. Recent
evidence suggests it may be even wider just at the V1 level alone. Specifically, neurons in
the superficial layer of V1 (the layer of cells closest to the surface of the brain, also known as
layer 1) appear to combine outputs from deeper V1 cells, to produce responses to particular
angles and junction types. Indeed, such cells make up about half of the neurons in the
superficial layer (Tang et al., 2018). Perhaps it should not be surprising that it codes such
complexity, because the superficial layer is mostly composed of dense connections with other
cells (Schmolesky, 2018) allowing information to be pooled.
Two problems must be solved early on in pattern recognition. These are (a) how to extract
an object from its background, known as the figure-ground segregation problem, and (b) how to
specify the object’s contour. These are closely related problems, because segregating figure
from ground requires identifying an object’s contour among visual clutter.
In monkeys, and presumably in humans, figure-ground segregation begins in V1 with
cells that combine the outputs of edge-sensitive feature detectors. This allows the de-
tection of boundaries and is followed by a “filling in” of the figure relative to the ground,
i.e., an enhancement of its boundary accompanied by coloring of the interior. That
process increases in intensity as visual input passes from V1 to V2 and V3/VP (Lamme,
Rodriguez-Rodriguez, & Spekreijse, 1999; Seymour, Williams, & Rich, 2016). It appears
to finish when area LO feeds input back to V1/V2. It is so powerful that it can extract a
contour when parts are missing or even when a contour is merely implied and not
physically present (see Figure 13.3; Wokke, Vandenbroucke, Scholte, & Lamme, 2013).
In humans, figure-ground segregation is better performed by the right as opposed to the
left hemisphere (Boles, 2002; Glezer, 1995).
Figure 13.3 Cells in V2 extract the contour of the implied (but not physically present) borderless triangle.
Source: Kanizsa triangle.svg, CC BY-SA 3.0, Fibonacci.
Similarities across species in the anatomy of V1 and V2 lead to the conclusion that both
derived from an early mammalian ancestor (Rosa & Manger, 2005). The distribution of V1 is
very wide among mammals including monotremes and marsupials, indicating an origin about
220 million years ago. V2 may have had later eutherian origins, about 170 million years ago
(Rosa & Krubitzer, 1999). Unfortunately, for the most part we do not know whether the
two areas play the same functional roles across distantly related mammalian species as they do
in primates. An exception is that since cats were used in the feature analysis experiments of
Hubel and Wiesel, it can probably be assumed that the sensitivity of V1 neurons to line
orientations has largely been preserved over the last 85 million years. However, an initially
disordered layout of neurons in V1 became orderly only about 80 million years ago in the
common ancestor of tree shrews and primates (Kaas, 2012).
General forms
From V2 a further processing step brings visual information to VP and V3 (also known as
V3v and V3d to emphasize their locations in the ventral and dorsal streams), as well as to V4.
All are involved in the processing of form, with evidence linking VP and V3 to dynamic
form, and V4 to color form (Kolb & Whishaw, 2009). Neurons in areas VP and V3 respond
to specific shapes at depths corresponding to the eyes’ fixation point and beyond, and also to
small objects embedded in clutter (Rosa & Manger, 2005).
The VP/V3 complex is found in both primates and non-primates, with at least traces
of it found in tree shrews, ferrets, and cats, but perhaps not in marsupials like the opossum.
At present, the best interpretation of the evidence is that like V2, VP/V3 originated with
eutherian mammals about 170 million years ago (Rosa & Manger, 2005).
Studies of form recognition are hampered by the virtually infinite variety of forms that
could be used as stimuli. Finding a shape that evokes a strong neuronal response doesn’t
preclude the possibility that another shape might evoke an even stronger response (Ponce
et al., 2019). Nevertheless using a large variety of shapes often enables the identification of
feature combinations to which a cell is sensitive. In macaque area V4, some cells are sensitive
to particular curvatures at particular orientations relative to an object’s center. An example
might be a concave curve to the left of center.
However, other cells in V4 are sensitive to certain combinations of multiple curvatures, that
can include other features. These cells respond to fairly specific objects such as an enclosed
form of a particular color and texture (Pasupathy et al., 2019). A simple example is a red
“squashed raindrop” (Pasupathy & Connor, 2002). More complex objects detected in V4
can combine many features and be quite difficult to characterize (Ponce et al., 2019).
Even so, it is probably the combination of features that evokes the response, not the object
itself, so that other objects with similar features would evoke a similar response. Thus, there is
nothing special about a red squashed raindrop beyond its particular assemblage of features.
Other objects with different features would evoke a response in other V4 cells. If nothing
else, this illustrates the subtlety of information coding in the ventral stream: At any particular
point in processing, representations may not match up closely with what we end up per-
ceiving, i.e., specific objects, but rather with abstract combinations of features.
V4 builds upon earlier contour processing by combining parts of an object (Pasupathy &
Connor, 2002), thus achieving a generalized, abstract representation of it. The area also
resolves depth information passed along from areas V1 and V2. Presumably this is in the
service of developing a 3D representation so that the abstract object can be perceived in
depth (Verhoef, Vogels, & Janssen, 2016).
Tracing the evolutionary origins of V4 is complicated by uncertainty in identifying cor-
responding locations in monkeys and humans. While a color-sensitive V4 exists in both
humans (Hong & Tong, 2017) and macaques (Pasupathy & Connor, 2002), the evidence for
homology is ambiguous at a neuroanatomical level (Orban, Van Essen, & Vanduffel, 2004).
In any case, little if any effort has been devoted to uncovering the origins of V4 prior to the
divergence of Old World monkeys.
A stronger case for homology can be made for the next cortical stage of pattern re-
cognition beyond V4. This involves a correspondence between inferotemporal (IT) cortex in
macaques and the “lateral occipital complex” (LOC) in humans. Human lateral occipital
(LO) cortex, illustrated in Figure 13.1, is usually considered part of LOC (Denys et al., 2004).
However, LOC also includes posterior portions of the inferior temporal gyrus (see
Figure 10.3) as well as the middle fusiform gyrus on the underneath side of the cortex. That
allows it to be characterized as a large area straddling the border between the occipital and
temporal lobes (Denys, et al., 2004).
The human LOC appears to be homologous with the monkey IT, both anatomically
(Denys et al., 2004; Orban et al., 2004) and functionally. Functionally, both areas respond
similarly to two-dimensional, three-dimensional, and moving patterns. Also, both show a
tendency to respond less in their anterior portions than in their posterior portions to
scrambled patterns, indicating increasing sensitivity to complex combinations of features as
processing moves forward in the brain (Denys et al., 2004). In this respect, IT and LOC both
resemble the function of area V4, differing from it in that larger proportions of their cells
show sensitivity to complex feature combinations (Tanaka, 1997).
Assuming that IT and LOC really are homologous, what is their evolutionary history?
Human LOC appears to have a greater monopoly over form processing than macaque IT, in
that the macaque parietal lobe also participates in recognizing visual form (Denys et al., 2004).
While this could indicate decreased specialization of brain areas in macaques relative to
humans – thereby “spreading out” processing to a larger degree – contrary observations apply
to the processing of motion and form. There monkeys show less overlap between motion and
form processing areas than do humans, suggesting increased specialization of brain areas.
The answer to this apparent contradiction may lie with tools. Specifically, habitual tool use
requires the integration of motion with two- and three-dimensional representations of tools,
potentially accounting for the greater overlap of motion and form processing in humans
(Denys et al., 2004). Viewed in this way the greater overlap is actually an indication of
increased specialization for tool use. Of course even if this explanation is correct, it is difficult
to say to what extent the species difference is due to human evolution, or to dissimilar tool
traditions – i.e., differences in learning.
Objects
We have seen that information accumulates about objects as visual input passes in a forward
direction from V1 on through the monkey IT and human LOC areas. The next step is to
achieve specific neural responses to specific concrete objects.
One possibility is that a given neuron in monkey IT cortex uniquely responds to a specific
object. To early researchers this seemed quite plausible, because one of the most striking
characteristics of the ventral system was the specificity that many cells seemed to exhibit. In
the early years of research on the ventral “what” pathway, such neurons were called gnostic
cells. Subsequently they became popularly known as grandmother cells because a single cell
might specifically respond to one’s grandmother (Bowers, 2017; Gross, 2002).
An alternative to grandmother cells is a distributed network of neurons that produces a
specific response to a particular object only as a population. According to this formulation,
each cell within the network responds to a wide variety of objects, but every object produces
a unique pattern of activation of some cells and not others.
In fact both of these possibilities are problematic. For grandmother cells, one problem is
that there would need to be a specific cell for every possible object we can recognize, itself a
mind-boggling prospect. In addition, the cell would somehow need to respond to that object
regardless of orientation, size, and color (Gross, 2002). Perceptual invariance is the ability to
recognize an object regardless of those and other physical transformations. While it is an
important achievement of the ventral “what” system operating as a whole, it seems unlikely
that a single cell recognizes a single object in all of its possible transformations.
For distributed networks, the major problem is that a network by itself does not seem well-
suited to assess its own state. For example, how can the network decide which specific object
corresponds to a particular pattern of activation across cells, unless there is a cell to recognize
each pattern of activation – in other words, a grandmother cell?
No current solution provides neat answers to these problems, but there are suggestions that
the key to object recognition lies somewhere between the extremes of grandmother cells and
fully distributed networks. Hung, Kreiman, Poggio, and DiCarlo (2005) combined an ar-
tificial intelligence application and single-cell recordings to estimate the number of IT
neurons needed to recognize an object. They recorded responses to 77 different objects from
300 neurons and fed them in varying numbers into a mathematics-based computer program
that in turn “learned” to recognize the objects from the neural responses. It was found that
reasonably high performance (72% correct) could be achieved by feeding 256 responses into
the program. This result suggests that assemblies of IT neurons numbering in the hundreds
are sufficient to achieve object recognition (Hung et al., 2005).
Even in this approach, however, the “grandmother” problem was alive and well, because
in the artificial intelligence implementation, each of the 77 objects had a “classifier” – in
effect, a grandmother cell – to determine whether an identification could be made. On the
other hand, an important feature of the study was that good performance was obtained even
when object position or size changed (Hung et al., 2005). Together these observations in-
dicate the potential feasibility of a hybrid solution that combines a distributed network to
achieve perceptual invariance, thereby greatly reducing the number of object instances that
must be recognized, together with grandmother cells to identify that reduced number.
It seems intuitively obvious that perceptual invariance must be achieved at a relatively
“high” level of the system, following substantial integration of neural activity. Studies of
brain activity support this intuition. Within both macaque IT and human LOC, the more
anterior sectors, at the furthest remove from earlier stages of processing, show the greatest
perceptual invariance. However, only a subset of cells in these areas achieve invariance,
indicating that the object recognition system maintains both invariant and variant re-
presentations of objects (Kovács et al., 2003; Sawamura, Georgieva, Vogels, Vanduffel, &
Orban, 2005). Again this makes intuitive sense, because we can clearly differentiate among
views while simultaneously recognizing that they are of the same object.
The increased integration of neural activity as processing proceeds forward within
IT/LOC cortex leads to an expectation that information should become increasingly
integrated across sensory modalities as well. In fact cells in the LOC area have been
found to respond to objects presented not just visually but also tactilely (Hernández-Pérez
et al., 2017). However, they are in the minority, and it seems more appropriate to
characterize LOC as making available a wide range of representations of objects. These
include (a) specific objects of specific position, size, viewing angle, contrast, and/or
texture; (b) specific objects independent of such factors or even of modality; (c) generic
objects of a general shape and color; and even (d) generic objects of no particular shape
and color (Desimone et al., 1984). Presumably the development of a wide variety of
representations is in the service of ultimately achieving, by way of their integration,
unambiguous recognition of the object.
Processes within IT/LOC appear to be evolutionarily well conserved, with an origin
sometime prior to 29 million years ago. However, the usefulness of this conclusion is limited
by the absence of other comparative data that could put a more definitive limit on the
emergence of the area.
Object classes
Recognizing an object as a unique instance of a larger class, e.g., your grandmother as
a member of the class of people, is aided by specializations of the ventral stream that are
class-specific. Particular subareas within the occipito-temporal cortex appear to be sensitive
to particular object classes such as faces or letters. Thus, the human fusiform gyrus, par-
ticularly in the right hemisphere, is sensitive to faces. In part this is known because of
single-cell recordings from patients in whom electrodes were implanted to localize the
source of epileptic seizures. A face recognition “patch” was found to be located largely,
though not exclusively, in the lateral and posterior portion of the fusiform gyrus (Allison,
Puce, Spencer, & McCarthy, 1999). A similar area appeared to be involved in recognizing
facial expressions such as happy, sad, and fearful (Li, Richardson, & Ghuman, 2019). Other
patches in the fusiform gyrus and its vicinity proved responsive to objects such as cars,
butterflies, flowers, and letters (Allison, et al., 1999).
The important question, of course, is whether particular patches are sensitive to specific
object classes and not others. This seemed to be the case in the study by Allison et al. Across
participants, face patches were generally located anterior to object patches, and letter patches
were located near the occipitotemporal sulcus as compared to the fusiform location of face
patches. Additional evidence that face patches are face-specific was reported in an fMRI
imaging study by Rhodes, Byatt, Michie, and Puce (2004), using lepidoptera (butterfly and
moth) experts. They found little overlap in the specific locations activated during lepidoptera
recognition and face recognition tasks, even though both tasks used the fusiform gyrus.
McCarthy, Puce, Belger, and Allison (1999) examined the effects of altering faces on the
response of face-specific patches in epileptic patients. Patch responses didn’t vary across color
versus black-and-white renditions of faces, or to larger versus smaller sizes, indicating that
they responded to faces irrespective of color or size. The patches also responded to cat
and dog faces, with reduced sensitivity. Inverting human faces (turning them upside down)
likewise reduced their response, more so in the right hemisphere than the left. Because
inversion presumably impacts the configuration of a face more than its features, the result was
viewed by the authors as implying configural processing of faces in the right hemisphere, but
piecemeal processing of faces in the left hemisphere. Finally, there were strong indications
that internal parts of faces like the eyes, nose, and mouth, were separately processed from
the full face, at sites close to the face patches.
Visual agnosia
Varieties of visual agnosia, the inability to recognize objects presented visually, likewise
support the existence of cortical patches that are sensitive to particular object classes. Cases
have been reported in which the recognition of living things is deficient even though
nonliving things are identified normally. The opposite has also been reported (Humphreys &
Forde, 2001). Other object classes sometimes showing deficient recognition, while other
classes are preserved, include faces, tools, animals, and fruits and vegetables (Capitani,
Laiacona, Mahon, & Caramazza, 2003; Tranel, Damasio, & Damasio, 1997).
Prosopagnosia is the name given to face-specific visual agnosia. It is typically due to lesions
of the fusiform gyrus, usually in the right hemisphere (Kanwisher & Yovel, 2006). Tranel and
colleagues have reported lesion data indicating that deficits in recognizing tools, faces, and
animals involve damage to differing portions of temporal cortex, although in some cases
occipital and parietal areas are also involved (Tranel et al., 1997).
Comparisons between species

The localization of object class patches appears to be similar in humans and monkeys.
Macaques have face-specific patches of inferior temporal cortex (Lafer-Sousa, Conway, &
Kanwisher, 2016), and direct stimulation of their IT cortex results in a biasing of decisions
toward seeing faces and away from seeing nonfaces (Afraz, Kiani, Esteky, 2006). However,
their face patches are less widespread than those in humans, perhaps because of cortical
expansion during human evolution that pushed some of them in the ventral direction (Lafer-
Sousa et al., 2016). Face patches are also seen in marmosets, which are New World monkeys
(Hung et al., 2015).
Furthermore, just as humans have difficulty recognizing upside-down faces, presumably
due to the disruption of configural information (see the Thatcher illusion in Figure 13.4), so
do chimpanzees, macaques, and New World monkeys (Calcutt, Rubin, Pokorny, & de
Waal, 2017; Taubert, Van Belle, Vanduffel, Rossion, & Vogels, 2015; Wilson & Tomonaga,
2018). However, the effect of inversion may be weaker and more methodology-dependent
in monkeys than in apes (Parr, 2011).
Crows and pigeons, in contrast, fail to show a face inversion effect (Brecht, Wagener,
Ostojic, Clayton, & Nieder, 2017). However, sheep recognizing other sheep do show the
inversion effect. Strikingly, like humans they also show a right hemisphere advantage in
recognizing faces, and as face familiarity increases, they become less sensitive to features and
seem to use more configural information (Peirce, Leigh, daCosta, & Kendrick, 2001; Peirce,
Leigh, & Kendrick, 2000).
These results suggest that primate taxa diverging from one another as far back as 44 million
years ago inherited a configuration-based and orientation-specific face recognition system
from a common ancestor. The sheep data suggest that this system dates back at least
85 million years ago, but the bird data suggest it postdates 300 million years ago. However,
orientation specificity may have strengthened in apes, including humans.
Global versus local bias

Viewing the Thatcher illusion, we only sense that something is catastrophically wrong when
the faces are in their familiar upright configurations, not when they are inverted even though
the same feature distortions are present. The illusion suggests that we are more sensitive to
configural distortions than we are to featural ones.
Could it be, then, that we are generally more sensitive to global configurations than we are
to features? Experiments using hierarchical stimuli (Figure 13.5) suggest that we are. In the
typical experiment, participants are asked to recognize either a large global letter or small
local ones, with either conflicting or neutral (“+”) information at the other level. Thus, in
two conditions of the typical experiment, participants are asked to recognize a global letter,
and are given either conflicting or neutral stimuli (left and center examples). In the other two
conditions, they are asked to recognize the local letters, and again are given either conflicting
or neutral stimuli (left and right examples).
Two major findings emerge from such studies (Figure 13.6). First, the global level is
responded to faster than the local level. Second, having conflicting information at the other
level slows local level responses more than it does global responses. Together these two
phenomena are sometimes called the global precedence effect because both presumably result
Figure 13.4 The Thatcher illusion, so named because the original illusion used pictures of British Prime
Minister Margaret Thatcher. Examine the pictures, then turn the page upside down and re-
examine them.
Source: Thatcher.PNG, public domain, Albert Kok.
H
A A + + H
A A + + H
A A + + H
A A A A A A + + + + + + H H H H H H H
A A + + H
A A + + H
A A + + H
H
Figure 13.5 Illustration of hierarchical stimuli. Left: Conflicting, Center: Global neutral, Right: Local
neutral. As shown, in the neutral conditions a nonletter plus sign substitutes at one level.
Figure 13.6 Mean RTs to the hierarchical stimuli.

from the faster processing of global information. Thus, if the global level provides conflicting
information, it interferes more because of its earlier availability. These basic results have been
replicated many times (e.g., Blanca & López-Montiel, 2009; Boles, 1984; Boles & Karner,
1996; Dale & Arnell, 2013).
Global and local processing in other primates

Similar hierarchical stimuli have been used to study pattern recognition in several primate
species. Hopkins and Washburn (2002) presented a match-to-sample task to common
chimpanzees, first showing as the sample a hierarchical letter stimulus, followed by the
same hierarchical stimulus as the target and a different hierarchical stimulus as the foil.
The task was to select the matching target while rejecting the foil, which could differ
from the sample at the global level, the local level, or both. Essentially, reaction time
reflected the time to reject the mismatching level or levels. It was found that the chim-
panzees rejected the global level more quickly than they did the local level. However,
when the same task was given to rhesus macaques, no difference was found between
global- and local-level rejections.
Fagot and colleagues used a somewhat different stimulus set and task for humans, chim-
panzees, and baboons (Fagot & Deruelle, 1997; Fagot & Tomonaga, 1999). Although the
results depended somewhat on other experimental manipulations such as the size and sparsity
of the display, the general result was that humans rejected the global patterns faster than the
local patterns, chimpanzees showed little difference, and baboons rejected local patterns faster
than global patterns. However, a followup study found that chimpanzees rejected global
patterns faster than local ones when the global pattern was made more salient (Fagot &
Tomonaga, 1999).
Finally, capuchins and tamarins have been subjected to similar testing, and have been
found to make faster or more accurate local rejections than global rejections (De Lillo,
Palumbo, Spinozzi, & Giustino, 2012; Neiworth et al., 2014; Truppa, De Simone, & De
Lillo, 2016). One study of capuchins even addressed the interference of one level on another.
Thus, Spinozzi, De Lillo, and Salvi (2006) used hierarchical stimuli in a matching-to-sample
study, with global matching and local matching performed on separate days. Percent errors
rather than reaction time was the measure, and the results are shown in Figure 13.7.
Although little difference was found between global and local matches when stimuli were
consistent, a big advantage of local matches was revealed when stimuli were conflicting. This
indicates interference of conflicting information at the local level on global matches, but not
vice versa, opposite to the human results of Figure 13.6. Capuchins appear to show not a
global but a local precedence effect.
Looking across all of these comparative studies, it appears that the modern human bias
toward global visual patterns is reflected at least partially in chimpanzees, but that Old World
monkeys (baboons and macaques) and New World monkeys (capuchins and tamarins) have a
Figure 13.7 Capuchin percent errors to hierarchical stimuli.

reversed, local bias. The data indicate that a quite striking evolutionary shift has been oc-
curring since we diverged from Old World monkeys 29 million years ago, extending past the
chimpanzee-human common ancestor 7.5 million years ago.
What exactly was it that shifted? Fagot and Tomonaga (1999) attribute the species dif-
ferences to the greater ability of chimpanzees and humans, relative to baboons, to percep-
tually group stimuli into global forms. Recognizing global form in hierarchical stimuli like
those in Figure 13.5 (or for that matter, in Figure 13.3) exploits the proximity and continuity
of small elements to extract contours that don’t actually exist. This may be something that
bigger, more interconnected brains are better at, starting with those of chimpanzee size.
Certainly an enhanced ability to extract larger forms from loosely associated features
improves pattern recognition, especially when the larger contours are obscured. In our
evolutionary past, global bias may have improved the recognition of partially obscured prey
or predators. It may have aided navigation over global terrain covered by seasonally changing
local vegetation. It may even have allowed better global imagery of a planned tool being
assembled from local parts. Seeing the forest before the trees (Navon, 1977) had definite
advantages in many situations.
Other pattern recognition processes and areas

Cortical areas besides those along the V1-inferotemporal route also participate in visual
pattern recognition. For example, the superior temporal sulcus (see Figure 10.3) contains
other face-sensitive patches, and responds to visual cues communicating face and body
movement. In humans, moving faces produce activation in separate posterior, middle, and
anterior portions of the sulcus, primarily in the right hemisphere, while macaques show
activation primarily in the anterior portion, with little lateralization (Zhang et al., 2020).
The superior temporal sulcus also has a high proportion of “polysensory” cells that respond
not just to vision but to other senses as well (Allison et al., 1999; Desimone et al., 1984).
In both monkeys and humans, the intraparietal sulcus (Figure 10.3) may play a role
in cross-modal matching, e.g., in matching a visual shape to a tactile one (Grefkes, Weiss,
Zilles, & Fink, 2002). The LOC is also active during visual-tactile integration (Lacey, Tal,
Amedi, & Sathian, 2009). Perirhinal cortex (cortex located in the medial temporal lobe) appears
to play a role in extracting the meaning of polymodal object representations (Holdstock,
Hocking, Notley, Devlin, & Price, 2009).
Then too, the auditory and somesthetic modalities have their own pattern recognition
systems. These are mostly localized, respectively, in the superior temporal and parietal lobes.
The auditory system plays a primary role in language and will be further described in that
context in Chapter 15.
Conclusion
The “what” pathway supports much of our visual pattern recognition. Located in the
ventral portions of the occipital and temporal lobes, it initially uses both spatial frequency
and feature analyses. Cells in the superficial layer of V1 appear to combine features so that
they are sensitive to complex angles and junction types. By the time information has “fed
forward” and been processed in V2, figure has separated from ground, and contours have
been extracted. Areas VP and V3 (also known as V3v and V3d) enhance boundaries and
color them in.
Comparative analyses indicate that V1 originated about 220 million years ago with the
emergence of mammals, while V2 as well as VP/V3 originated about 170 million years ago
with eutherian mammals.
Neurons in V4 are sensitive to combinations of curvatures organized relative to an object’s
center, thus achieving a representation of an object’s combined parts. It also incorporates
depth so that a 3D representation is achieved. The next stage, involving the homologous
areas of the LOC in humans and IT cortex in macaques, seems to build on these re-
presentations through sensitivity to complex feature combinations.
The LOC/IT areas trace at least as far back as the emergence of Old World monkeys
29 million years ago, but little is known about their earlier origins. There seems to have been
some divergence between macaques and humans in that humans show an increased spe-
cialization of LOC relative to monkey IT, yet more integration of motion and form in-
formation. This may reflect increased specialization for tool use.
Recent research has estimated the number of inferotemporal neurons necessary to re-
cognize an object in the hundreds rather than the much larger numbers of a fully distributed
network. However, they don’t completely escape a problem associated with “grandmother”
cells, namely the need for a dedicated unit to recognize each object. On the other hand, a
strength is that networks can achieve a substantial degree of invariance, representing the same
object regardless of transformation in such physical characteristics as position or size.
Neurons at this level are organized into “patches” that are specific to object classes such as
faces, cars, butterflies, flowers, and letters. Face patches are largely though not exclusively
located in the fusiform gyrus, especially in the right hemisphere. Damage to this area can
cause prosopagnosia, a visual agnosia for faces. New World and Old World monkeys,
chimpanzees, humans, and even sheep all appear to have the same configuration-based,
orientation-specific mechanism for recognizing faces, something not shared by pigeons.
This suggests an origin at least 85 million years ago, but how much more recently than our
300-million-year-old common ancestor with birds is unclear.
Experiments using hierarchical stimuli indicate that humans are more sensitive to global
configurations than to features. We respond faster to the global level, and conflicting in-
formation at that level interferes more with feature processing than the reverse, two phe-
nomena that together are called the global precedence effect. Chimpanzees appear to show a
weaker form of the effect, while Old World and New World monkeys show an opposite,
local precedence effect. Thus, an evolutionary shift from local to global precedence may
have started about 29 million years ago, down to later than 7.5 million years ago. It may be
that bigger, more interconnected brains are better able to use the proximity of small elements
and their apparent continuity to extract global form.
14 Memory
Skilled handedness, tool use and manufacture, spatial perception, and object recognition have
something in common: They require a highly evolved ability to remember. In our day-to-
day lives, we constantly access information in memory that represents the meaning of
environmental stimuli. We use memory to select action and to execute it after recalling
learned motor patterns. In a real sense, memory can be viewed as a prerequisite for all
perceptual and cognitive activity.
In general, memory is defined as the ability to retain information from past events. It is
phylogenetically ancient in the form of habituation, a decline in response to repeated sti-
mulation. Even single-cell organisms show declining responses on repetition, e.g., by
ceasing contraction in response to repeated pressure changes in the surrounding water
(van Duijn, 2017). Because habituation involves retaining information from past events –
i.e., an event has occurred repeatedly in the past and so response is reduced – it qualifies as
a memory phenomenon, although a very primitive one (Moore, 2004; Szabo, Noble, &
Whiting, 2021).
A more restrictive definition of memory requires association, the arbitrary pairing of a
stimulus with a response. In classical conditioning, associations are learned when a condi-
tioned stimulus (e.g., a ringing bell) shortly precedes an unconditioned stimulus (e.g., meat),
which evokes a reflexive response (e.g., salivation in Pavlov’s dogs). Soon, the conditioned
stimulus itself produces the response without any intervening unconditioned stimulus,
showing that an arbitrary association has been learned between the stimulus and the response.
In theory, the same stimulus could arbitrarily be paired with any other response and con-
ditioned in similar fashion.
Association is what most people mean by memory. For example, when we learn a new
face, we learn arbitrary facts associated to the face: A name, that this is our new boss, that this
face’s office is down the hall. There is nothing “built in” or reflexive about any of those
associations; they have to be learned as arbitrary bits of information attached to a stimulus.
Like habituation, conditioning in various forms is phylogenetically ancient. It has been
observed in snails, wasps, and birds, as well as in kittens, lambs, rats, monkeys, and a host of
other mammals (Moore, 2004). It has even been observed in planaria (Hutchinson, Prados, &
Davidson, 2015), a flatworm whose common ancestry with our own traces back almost to
the origin of bilateria during the Cambrian explosion. It probably extends even before that,
as sea anemones show conditioning to both food and shock stimuli (Cheng, 2021). Because
sea anemones are cnidarians, conditioning likely traces at least to the cnidarian divergence
over 605 million years ago.
These observations may indicate the importance of nerve cells and their organization to
conditioning. Cnidarians, including sea anemones, have a diffuse neural net using un-
specialized neurons (Havrilak et al., 2017; Cheng, 2021). Planaria and some other flatworms
show greater neural organization, as well as a differentiation of neurons into sensory,
DOI: 10.4324/9781003137863-17
Memory 241
association, and motor types (Hickman, Roberts, & Larson, 1997). Thus, the presence of
nerve cells having at least net-like organization – but not necessarily specialization into
functional types – may be a prerequisite for conditioning.
One problem in uncovering the evolutionary origins of memory is the sheer variety in
forms of learning that have been investigated. Moore (2004) suggested that there are dozens
of biologically distinct kinds of learning, including ten different forms of conditioning.
However, his analysis proceeded largely on logical grounds, and it is unclear to what extent
so many different kinds of learning actually involve different abilities.
In any case, it seems indirect to trace memory’s evolutionary origins by examining learning
abilities rather than types of memory. Whether or not an animal learns using a particular
method is likely to depend on a number of factors. They include sensitivity to the stimuli
used, the ability to make the required response, and even the species’ predisposition toward
associating certain stimuli to certain responses and not others (Seligman, 1970).
Cognitive psychology offers a more direct approach by positing the existence of several
empirically dissociable memory stores, or kinds of memory. This structural approach eliminates
the problems of a learning-based approach by focusing on the nature and fate of the in-
formation that is remembered, not the method by which it became represented in memory.
For the most part, the approach taken here will be to describe each component of
memory from the human perspective, accompanied by a comparative analysis to identify
evolutionary trends.
Sensory memory
Sensory memory is a very short-lived trace that preserves much of the physical form of
stimuli and lasts at most several seconds. The visual form of sensory memory, known as
the icon, may be the best understood. It is a copy of visual stimulation that lasts half a
second or less in brightly lit conditions but up to four seconds in the dark (Sperling,
1963). An example is a sparkler waved in a circle in the dark (Figure 14.1). The resulting
smear makes the circle appear complete when in actuality, at any instant the tip of the
sparkler only emits a point of light on the circle. The icon is thus a very brief memory
that forms a bridge from one instant of time to the next, creating a continuous visual
experience. It is responsible for our sense of continuity when watching a 24-frame-per-
second Hollywood movie.
The peripheral component

The icon is due to the aftereffects of activity at various levels of visual processing, including
the periphery of the nervous system. Sakitt and Long (1979) established the retina itself as the
location of one component of the icon. In one of their experiments, the task was to judge the
location of a red dot on a gray background, determining the direction it moved between
successive frames. To perform this task, an iconic memory of the first frame had to be
matched to the second frame. Accuracy at the varying delays thus indicated the extent to
which information was still in the icon of the first frame.
Furthermore, the intensities of the dot and background were carefully adjusted so that in
one condition, the rods in the retina had a difficult time separating the dot from the back-
ground. Rods are sensitive to gray but insensitive to red, and do not differentiate between
colors, so an appropriate high-intensity red and a low-intensity gray effectively blind the rods
with respect to any difference. However, the cones can easily tell the difference, so this
condition was called the cone contrast condition. In these circumstances, the icon was found
Figure 14.1 A circle created with a sparkler. Points in the circle don’t persist over time, but instead are held
in sensory memory (or in this case, during the exposure interval of the camera) to create the
illusion of a circle.
Source: Sparkler Fun, CC BY-SA 2.0, Kirt Edblom.
to fade rapidly over 400 msec. Presumably, the cones in the retina were responsible for the
icon in this condition.
In the other half of the experiment, the rod contrast condition, the task was made difficult
for the cones by adjusting the intensities so that the dot and background appeared equally
bright to the cones. Although the cones could still detect a color difference, this condition
made it more likely that the rods would be involved in the task, and it certainly should have
been easier for the rods than the cones. In this condition, performance again declined over
400 msec, but to a much smaller extent implying that the icon was holding information for a
much longer time (Figure 14.2).
The beauty of these results is that they accord with what is otherwise known about the
duration of the icon. As already indicated, in brightly lit (daytime) conditions, it lasts only half
a second or less, while in dark (nighttime) conditions, it can last up to four seconds. Daytime
vision depends on the cones and nighttime vision on the rods, so the difference between the
cone contrast and rod contrast conditions accords well with that difference. Most im-
portantly, the results indicate that one component of the icon is located at the retina: The
cones are responsible for a rapidly fading version of it while the rods are responsible for a
more slowly fading version. Of course, the usefulness of the rod version is limited by the low
resolution of the rod system (Long & McCarthy, 1982).
Memory 243
Figure 14.2 Decay of the icon (with the curves smoothed for clarity) under rod and cone contrast conditions.
The central component

In contrast, there is also strong evidence of a brain-based, central component of the icon.
When a visual stimulus is presented briefly and is followed by a pattern mask – a second
stimulus that spatially covers the first and is composed of jumbled features – recognition of
the first is compromised. Furthermore, the mask is most effective not when it is presented
immediately after the stimulus, but when it is presented at a short delay of 30–100 msec
(Skottun & Skoyles, 2010). This result implies that the mask catches up to the stimulus at a
later, time-consuming stage of processing – i.e., feature analysis – and disrupts it (Box 14.1).
Most importantly, masking occurs even if the stimulus is presented to one eye and the mask is
presented to the other eye. Because inputs to the two eyes do not anatomically converge
until they reach the primary cortex, this result strongly implies that there is a central com-
ponent of the icon located in the brain. Furthermore, a different type of mask has different
effects: An unpatterned flash of light is most effective at a zero delay following the stimulus,
and only if it is presented to the same eye as the stimulus. Like the study of Sakitt and Long,
this implicates a peripheral, retina-based component of the icon (Breitmeyer, 1984).
Box 14.1 How can a mask catch up to an earlier stimulus?
A pattern mask is most effective when it is briefly delayed relative to the stimulus, a
result interpreted as the mask “catching up” to the stimulus at a time-consuming stage
of processing. But how is that possible? Logically, it seems that a delay should be
maintained throughout the processing system, so that the stimulus always stays ahead of
the pursuing mask.
The answer lies in a two-phase response of the visual system. The magnocellular
response is a rapid response to stimulation that preserves only fuzzy detail but serves to
alert the system to the appearance and location of the stimulus. The parvocellular response
is much slower, but contains detailed information that allows feature extraction and
identification of the stimulus. The two responses are transmitted by different, but
roughly parallel, systems of cells beginning in the retina.
It is the faster speed of the magnocellular system that allows a pattern mask to
“catch up” to a stimulus. The fast magnocellular response to the mask reaches feature
analyzers in the cortex at the same time as the slower parvocellular response to the
stimulus, even though the mask was presented after the stimulus. Consistent with this
explanation, if the task is simply to indicate the location of the stimulus without
identifying its features, a delayed pattern mask is not effective. In that case, the
magnocellular response to the stimulus does indeed stay ahead of the pursuing mask
( Öğmen, Breitmeyer, Todd, & Mardon, 2006).
Other forms of sensory memory that have been investigated include auditory sensory
memory, the so-called echo lasting about two to ten seconds (Bijsterveld, 2015), and a
somesthetic sensory memory lasting about one to two seconds (Bliss, Crane, Mansfield, &
Townsend, 1966).
The general interpretation that has been offered for the existence of all of these is that
they represent aftereffects of neural activity. With respect to the icon, the cones and rods of
the retina remain in a heightened state of activity for a brief period of time following
stimulation, preserving a sensory trace of the stimulus. The same is true of visual feature
detectors beginning with V1 in the cortex. With respect to the echo, durations toward the
lower end of the two to ten second range appear to be associated with residual activity in
the primary auditory cortex, while longer durations reflect activity in association auditory
cortex (Lu et al., 1992).
The evolution of sensory memory

It is evident from the discussion so far that the evolution of sensory memory must be closely
tied to the evolution of sensory receptors and a sensory brain. As we have seen (Chapter 7),
visual sensation has an ancient history, with cnidarians likely having the first eyes that
connected to neurons, as well as rhodopsin-based photoreceptors. Thus, the retinal com-
ponent of the icon probably traces back 605 million years.
The emergence of a brain component presumably waited, at minimum, on the evolution
of a strongly centralized nervous system, possibly as early as flatworms some 535 million years
ago. It is more probable, however, that our central component emerged with the evolution
of the primary cortical area V1, which, as we have seen, was a mammalian innovation dating
back about 220 million years ago. Certainly, masking occurs in Old World monkeys, e.g.,
with their perception of animal pictures disruptable by a pattern mask delivered 50 msec after
stimulus presentation (Cauchoix, Crouzet, Fize, & Serre, 2016).
Short-term memory
Short-term memory has a much smaller capacity but a much longer duration than sensory
memory. Whereas sensory memory preserves a copy of all stimulation for a few seconds at
most, short-term memory holds a maximum of about nine items for 20 seconds or so.
However, it may be refreshed indefinitely by rehearsal, e.g., when vocally repeating a phone
number from a contact list (Baddeley, 1986; Klatzky, 1980).
The capacity of nine items is a generalization that greatly depends on the type of item held
in memory. Capacity is measured by requiring that varying numbers of items be recalled in
the order presented. The number of items that can consistently be recalled in correct order is
the memory span. Strings of random digits (e.g., 3, 6, 1, 7) are subject to the “seven, plus or
Memory 245
minus two” dictum made famous by George Miller (1956). Five to nine digits can be re-
membered in order, depending on the individual and the conditions of the experiment.
Cavanagh (1972) reviewed the literature and found that average memory span varied de-
pending on the type of item: E.g., about eight for colors, five to six for random words, and
three for nonsense syllables.
Thus, short-term memory does not have a fixed number of “slots” but rather a fixed
capacity for information. Items requiring more detailed memory (e.g., random words and
nonsense syllables) have fewer slots than items requiring less-detailed memory (e.g., digits and
colors; Alvarez & Cavanagh, 2004; Cavanagh, 1972). Conversely, stretching capacity over
ever-increasing numbers of items results in a progressive degradation of memory content,
indicating that a limited information resource is being stretched too thin (Bays, 2018).
The informational view is lent weight by an orderly relationship between memory span
and search time through short-term memory. When several items are held in memory
(the memory set), reaction time (RT) to decide whether a subsequent probe was among the
memory set increases linearly with the number of items in the set. For digits, RT increases
about 33 msec per digit, implying that it takes that amount of time to compare the probe to
a single memory item. As it turns out, plotting the comparison time for a particular kind
of memory item against the memory span for that item results in a linear relationship. For
example, colors on average show a 38 msec comparison time and a 7.1 item memory span,
random words a 47 msec comparison time and a 5.5 item memory span, and nonsense
syllables a 73 msec comparison time and a 3.4 item memory span (Cavanagh, 1972). In other
words, memory span systematically decreases as comparison time increases. This result
supports the informational view of short-term memory because it implies that the greater
the detail required to remember an item, as reflected in the memory span, the more time is
required to compare the probe to an item in memory.
At least if held in auditory form, information in short-term memory generally lasts 10 to
30 seconds if it is not refreshed through rehearsal. That makes 20 seconds a reasonable
estimate of the duration of short-term memory (Klatzky, 1980).
Comparative studies of short-term memory

Wright and colleagues have reported that pigeons, rhesus macaques, and humans all have
short-term memories. They presented sets of four pictures as memory items, followed after a
delay by a single probe. Monkeys and humans moved a lever to the right or left, while
pigeons pecked right- or left-colored disks, depending on whether or not the probe was in
the memory set. It was found that all three species showed a recency effect in which the most
recent item or items in a list were recalled better than the list items immediately preceding
(Wright, Santiago, Sands, Kendrick, & Cook, 1985). This was an indication of the existence
of short-term memory, for the most recent items were presumably those most active in it
when the probe was presented.
Most importantly, Wright et al. found that the recency effect disappeared if the probe was
sufficiently delayed, implying that information had been lost from memory. This effect varied
across species. For pigeons, the recency effect was present with a probe delay of two seconds,
but absent at delays of six seconds or more. For monkeys, the recency effect was still present
at ten seconds but gone by 20 seconds; while for humans it was still present at 60 seconds but
gone by 100 seconds (Wright et al., 1985). The implication is that the species differed in
terms of (a) the duration of short-term memory, (b) the ability to rehearse information in
short-term memory, or (c) both. Thus, humans showed the longest-duration short-term
memory and/or the most-effective rehearsal process, while pigeons showed the shortest
duration memory and/or the least-effective rehearsal process. But, all showed evidence of
short-term memory.
There are probably also species differences in the capacity of short-term memory. Fagot
and De Lillo (2011) tested the ability of two baboons to reproduce the order in which squares
were presented at different locations on a screen. They performed better than chance to as
many as five items. Humans, however, were found to perform so far above chance that
capacity was well above six items, the maximum number used in the study.
Chimpanzees, too, appear to have a short-term memory. It lasts at least 15 seconds, is
limited in capacity to a few items, and while items are retained, is subject to interference
when other tasks are performed. All of these characteristics apply as well to human short-term
memory (Völter, Mundry, Call, & Seed, 2019).
If there are species differences in short-term memory duration, they may not follow a
phylogenetic progression. Lind, Enquist, and Ghirlanda (2015) compared multiple non-
human animals by drawing on more than 90 delayed matching-to-sample studies. In these
studies, a stimulus, typically visual, was followed after a delay by the same stimulus and an
accompanying distractor, and the task was simply to choose the match to the first stimulus.
Across studies, the duration of memory was found to be disordered across species. For
example, pinyon jays and capuchins showed an average duration of 39 seconds, while for
chimpanzees it was only 19 seconds. It is possible, however, that methodological differ-
ences between studies were responsible for disorderliness in the results (Lind et al., 2015),
a supposition that could be tested in future research by using a consistent methodology
across species.
Greater insight into the evolutionary origins of short-term memory may come from
considering its neurological underpinnings. Reviews of PET and fMRI studies conducted
with humans implicate a small number of cortical areas that vary somewhat depending
on whether auditory-verbal or visual-spatial short-term memory is considered (Andre,
Picchioni, Zhang, & Toulopoulou, 2016; Cabeza & Nyberg, 2000). For the former, most
studies show activation in left inferior parietal cortex (Brodmann area 40; see Figure 10.4)
and left or bilateral premotor cortex in the frontal lobe (areas 6 and 44). For visual-spatial
short-term memory, most have shown activation in bilateral superior parietal cortex (area 7)
and bilateral premotor cortex (area 6). In addition, auditory-verbal and visual-spatial short-
term memory both appear to involve left area 10.
Of these, areas 40 and 7 are most consistent with the storage component of short-term
memory, with left area 40 storing phonological representations of memory items, and
bilateral area 7 storing visual–spatial representations (Cabeza & Nyberg, 2000).
Working memory
But what about the area 6, 44, and 10 activations? These may best be understood by con-
sidering the concept of working memory developed by Alan Baddeley (1986). Working
memory incorporates the storage aspects of short-term memory by proposing the existence of
an “articulatory loop” in which information may be held through the process of verbal
rehearsal (i.e., area 40), and a “visuo-spatial sketch pad” in which information may be held in
a visual format (i.e., area 7). Both are subordinate to a reasoning, active component of
working memory called the “executive control system”, that can consciously manipulate
their contents. By this view, the area 6 activation corresponds to activation in the executive
control system. Support for this role comes from research linking area 6 activity to problem
solving (Fincham et al., 2002), reasoning (Monti & Osherson, 2012), and short-term in-
formation updating (Nee & Brown, 2013). Area 6 is part of a larger frontal lobe network
Memory 247
involved in executive control, for as we have seen, area 10 appears to evaluate the contents of
working memory (see Chapter 11). Left area 44, on the other hand, constitutes a portion
of Broca’s area. Activation there likely corresponds to the verbal rehearsal component of
working memory (Cabeza & Nyberg, 2000).
In contrast to area 6 and 44 activations in humans, macaque working memory activations
are generally in areas 9 and 46 (Petrides, 2005; Petrides & Pandya, 1999). Frontal lobe
homologies between humans and macaques are close (Figure 14.3), so these really appear to
be different areas of activation than those most frequently observed in humans. However,
areas 9 and 46 do activate in a fair number of human working memory studies (Cabeza &
Nyberg, 2000). It seems possible that they comprise an evolutionarily older substrate for
working memory, dating back to at least a macaque-human common ancestor 29 million
years ago, and that during human (or possibly ape) evolution, adjacent areas (i.e., 10 and 44)
and nearby areas (i.e., 6) have been recruited.
In any case it is clear that in monkeys and humans, short-term memory is based in the
neocortex. Birds including pigeons do not have a structure homologous to the neocortex of
mammals (Krauzlis, Bogadhi, Herman, & Bollimunta, 2018). Thus, short-term memory in
birds on the one hand, and primates on the other, is best regarded as a matter of convergent
evolution.
Intermediate-term memory
Mark Rosenzweig and colleagues have called attention to an intermediate-term memory
in certain animals (Rosenzweig, Bennett, Colombo, Lee, & Serrano, 1993). For example,
after chicks are trained to avoid pecking a normally attractive shiny bead, their avoidance
initially dips over time, then recovers (Figure 14.4). The result is consistent with the
phasing out of an intermediate term memory, succeeded by long-term memory
(Rosenzweig et al., 1993).
Somewhat similar findings have been reported from the nautilus, a deep-water shelled
mollusk. The animals were conditioned to extend their tentacles following presentation of
a signal light, and they were subsequently tested at intervals. Memory declined smoothly
over one hour, but dramatically rebounded after six hours (Crook & Basil, 2008).
Intermediate memories with varying temporal characteristics have also been proposed for
fruit flies, honeybees, roundworms, snails, and sea hares, a type of sea slug (Braun &
Likowiak, 2011).
The idea of an hours-long memory intermediate to what in humans is a seconds-long
short-term memory and a decades-long long-term memory is certainly appealing.
However, to this point there is no evidence for it in people. Human memory follows a
smoothly declining trajectory (Figure 14.5), to the extent that detecting any discontinuity
at all, let alone a dramatic rebound, is somewhere between difficult and impossible (Rubin,
Hinton, & Wenzel, 1999; Wickelgren, 1973). In addition, it smoothly declines regardless
of whether the memory items are nonsense syllables, words, pictures, or geometric forms
(Gilliland, 1948; Wixted & Ebbesen, 1997). That means that the human–animal difference
cannot be attributed to the predominant use of verbal memory items in human research on
forgetting.
Therefore, it appears that intermediate-term memory has no parallel in humans. Perhaps
the necessary mutations never occurred, or perhaps they occurred and were subsequently
selected against. Presumably a smooth forgetting function improves estimates of when events
occurred and in what order, an important capability for a species dependent on experiential
recollection. That could be a possible reason for deselection of an intermediate-term
memory.
Figure 14.3 Brodmann areas in human frontal cortex (a), and corresponding areas in macaques (b).
Source: Architectonic map of the human and macaque monkey prefrontal cortex, CC BY-SA 4.0, M. Petrides, D.N.
Pandya.
Memory 249
80
60
% Avoidance
40
20
0
1 15 30 60 90 120
Interval since training (min)
Figure 14.4 Avoidance in chicks following training, showing recovery of memory over 120 minutes and
thus implying the existence of an intermediate term memory.
Figure 14.5 Example of the human forgetting function, showing a smooth decline of percent correct recalls
over time. Note the contrast with Figure 14.4.
Long-term memory and its divisions
If association is what most people think of when they think of memory, long-term memory
is its primary repository. In this form of memory, knowledge and experiences can be retained
more or less permanently. Models of human cognitive processing hold that information
enters long-term memory from short-term memory through rehearsal. Maintenance rehearsal
(rote repetition) suffices to increase a sense of familiarity of memory items, but elaborative
rehearsal is required to embed memory items firmly enough in long-term memory to allow
their recall. Elaborative rehearsal involves processing the meaning of the items, thus asso-
ciating them to the existing knowledge structure (Klatzky, 1980).
Long-term memory actually refers to a family of memory systems. Most comparative
research, however, has explored two divisions of long-term memory called episodic memory
and semantic memory. Episodic memory is literally memory for episodes or particular events in
the past, while semantic memory is memory for the facts that make up our knowledge
structure.
A distinction between these systems is strongly indicated on neurological grounds.
Amnesic patients who have suffered damage to the hippocampus and neighboring areas of
the brain show severely impaired encoding of new information into episodic memory, while
simultaneously showing a relative sparing of the acquisition of new semantic information
(Rosenbaum, Gilboa, & Moscovitch, 2014). For example, a patient with amnesia may not
remember a trip to Florida taken last year, while simultaneously recalling that the capital of
Florida is Tallahassee, a fact learned during the trip.
Brain imaging and lesion studies also indicate a difference between episodic and semantic
memory. For episodic memory, encoding a new event most often activates the medial
temporal cortex, where the hippocampus is located, but retrieving an event most often in-
volves area 10 of the frontal lobe (Cabeza & Nyberg, 2000). Lesions affecting episodic
memory also typically involve the medial temporal lobe, especially the hippocampus
(McCormick, Ciaramelli, De Luca, & Maguire, 2018).
In contrast, semantic memory retrieval involves the lateral temporal cortex. It also in-
volves area 45 of the frontal lobe in both encoding and retrieval; however, this may be
specific to tests that are verbal in nature, calling on language-related structures (Cabeza &
Nyberg, 2000).
Lateral temporal involvement was confirmed in a study relating activation in normal brains
responding to semantic tasks, to the site of brain atrophy (shrinkage) in semantic dementia. In
semantic dementia, use of semantic knowledge is impaired while episodic memory is spared.
The study found the activation and atrophy sites to be the same: The anterior lateral temporal
lobe, in both hemispheres. More specifically, the activation data implicate the anterior
portions of the middle and superior temporal gyri (see Figure 10.3; Rogers et al., 2006).
Others have confirmed that this area is among those affected in semantic dementia (Landin-
Romero, Tan, Hodges, & Kumfor, 2016).
Episodic memory
Do animals have episodic memories? Hampton and Schwartz (2004) have emphasized how
difficult they are to demonstrate. Because animals lack language, memory is generally tested
with recognition tasks in which previously seen items are picked from an array of such items
intermixed with distractors. Because the items were learned as an episode, it is true that
episodic memory could be responsible for correct recognitions. But unfortunately, mere
familiarity could also support recognition. Good performance might therefore result not from
recall of the learning episode, but from a vague feeling that items have been seen before.
Memory 251
A second problem was noted by Schwartz, Hoffman, and Evans (2005) in regard to
previous research by Menzel (1999). In Menzel’s study, a chimpanzee indicated the nature
and location of hidden food to human caregivers, having observed it being hidden up to
16 hours previously. While that could certainly be an indication of episodic memory, it could
also be that semantic memory was employed, and that the chimpanzee merely indicated what
it knew to be true (i.e., that there is a particular food item hidden over there), without any
specific recall of the episode of the food being hidden.
Therefore, turning this observation on its head, one way of demonstrating episodic
memory might be to require the recall of something that was once true and was learned
through a single observation, but which should be known by the recaller to no longer be
true. For example, as I write this, I can recall being at the library earlier in the day and seeing
a particular book on a shelf; it was true then but is no longer true, because I checked it out
from the library. My memory must be of an episode, since it is not a truth represented in
semantic memory.
This kind of strategy has been employed in a series of studies of a lowland gorilla named
King. In the initial study, King was trained to respond to the English question, “What did
you eat?” by handing over a card symbolizing one of five kinds of fruit. Subsequently he was
given the corresponding piece of fruit, and at either a short delay (5–65 minutes) or a long
delay (24–96 hours) was asked what he had eaten. At both delays, he was 70–80% correct,
well above chance performance. In a second study, he was able to indicate both the food
eaten and the person who had given it to him, at both short and long delays. Thus, in both
studies, King recalled information learned in a single trial, that he should have known to no
longer be true: He had eaten the food, so it existed only as a memory (Schwartz, Colon,
Sanchez, Rodriguez, & Evans, 2002).
Of course, it is always possible that King based his responses not on recalled episodes, but
rather on a sense of familiarity evoked by the most recently-presented fruit or the most recent
human benefactor. Familiarity was perhaps most convincingly ruled out in one of a later set
of studies (Schwartz et al., 2005). King was given three pieces of fruit one at a time, at five-
minute intervals, e.g., apple-grapes-pear. During training, after five minutes he had to
produce the three cards that symbolized the fruit, in reverse order, i.e., pear-grapes-apple,
and if successful, he was given raisins. Subsequently, once this procedure had been learned,
King was tested at longer intervals (5–23 minutes) and was successful (Schwartz et al., 2005).
Mere familiarity could not have been the basis for his performance, because it could not
plausibly have provided sufficient information to correctly order multiple cards. Thus, King
appears to have an episodic memory.
Different researchers have adopted different criteria for demonstrations of episodic
memory, but the requirements that learning (a) be achieved in one trial, (b) reflect cir-
cumstances the animal should know are no longer true, (c) persist over intervals of at least
several minutes, and (d) produce recognition that cannot plausibly be attributed to familiarity
alone, would seem sufficient to convince most observers that episodic and not semantic
memory is involved. Unfortunately, it is a very difficult combination to satisfy.
A revealing study, but one that only partially satisfied the four conditions, was con-
ducted by Lewis, Call, and Bemtsen (2017) using a relatively large sample of 33 apes
(chimpanzees, orangutans, and bonobos). The apes witnessed an experimenter showing
them food that was not part of their regular diet, and then observed the experimenter
hiding it in a concealed location after climbing a ladder. The animals were given im-
mediate access to the enclosure, and those that succeeded in climbing up to and finding the
food in less than five minutes were included in the subsequent study. In that study, at a
delay of 2, 10, or 50 weeks, the ape entered the enclosure and discovered the same kind of
food on the ground below the hiding place. The question was whether the animal would
Figure 14.6 Percentage of climbs in the hidden food study, as a function of retention interval.
then climb the ladder to search the previous hiding place. The answer was a resounding
yes, but with an apparent delay effect such that the longer the delay, the fewer the climbs
(Figure 14.6; note, however, that the delay effect was nonsignificant). Furthermore,
control animals that had not been exposed to the initial food hiding did not climb
the ladder.
The study certainly satisfied condition (a), one-trial learning, and (c), persistence. It
probably satisfied condition (b), because the animals had previously eaten the food stored in
the hiding place. It did not satisfy (d), however, because familiarity alone could plausibly have
led animals to climb the ladder. In spite of that, the results are revealing because one-trial
learning persisted at a respectable level even 50 weeks after the episode. In addition,
something resembling the human forgetting function was seemingly obtained.
Scrub jays show evidence of memory satisfying all four of the episodic memory criteria, as
well as correctly recalling “what”, “where”, and “when” information about hidden food
(Hampton & Schwartz, 2004). The “when” aspect is particularly intriguing because the jays
avoid looking for food hidden sufficiently long ago that it should be spoiled.
In one of the best designed of these studies, the birds were first taught that cached
worms (a preferred food) degraded over time, while nuts remained intact (Clayton, Bussey,
& Dickinson, 2003). They then were allowed to cache worms and nuts, on separate sides
of a tray and on separate days. Later, they were required to choose a side, with the food
removed. At short delays, the task was to choose the side in which the worms had been
cached, but at long delays the side in which the nuts had been cached. The jays were able
to perform this task successfully, seeming to satisfy the criteria developed earlier. Thus,
caching a particular food was a one-time act; preferentially avoiding worm locations after a
long delay indicated an understanding that circumstances had changed (i.e., the worms had
degraded); the delay of hours-to-days showed long persistence; and familiarity could not
account for the results since the worm and nut locations were equally familiar. Such
memories indeed seem episodic.
Subsequent to the research on jays, a similar experiment was conducted with a mixed
group of bonobos, common chimpanzees, and orangutans. Frozen juice and grapes were
the perishable and nonperishable foods, with the juice irretrievably melting through a net
over the space of an hour. After training, the animals were shown both being hidden, and
were then allowed to choose and access one location at 5- or 60-minute delays. It was
found that a strong preference for the frozen juice location at the short delay was
Memory 253
substantially reduced at the longer delay, similar to the scrub jay results. Interestingly, there
was a relationship between delay effect and the animals’ age, with only those of middling
age (10–14 years) showing a substantial reduction in frozen juice choices at 60 minutes
(Martin-Ordas, Haun, Colmenares, & Call, 2010).
Somewhat similar studies have been carried out in rats, and they implicate the hippo-
campus in animal episodic memory (Eichenbaum and Fortin, 2005; Naqshbandi, Feeney,
McKenzie, & Roberts, 2007). Thus, Eichenbaum and Fortin (2005) reported studies in
which rats were exposed to five odors, then were required to discriminate which of two test
odors had been presented prior to the other. Normal rats succeeded, but rats with hippo-
campal lesions failed. Importantly, both the normal and lesioned rats were able to perform the
simpler task of recognizing which of two odors had been presented in the five-odor series,
with performance declining for odors presented earlier in the series. This result indicates that
both groups of rats had access to a memory trace that faded over time, but only the normal
rats were able to use the trace in episode-like fashion: They correctly picked the earlier-
presented odor in a pair even though more forgetting had occurred for it. While the degree
of control over familiarity is not as good in this paradigm as in the jay paradigm – after all, the
task could conceivably be performed by selecting the less familiar alternative – the in-
volvement of the hippocampus provides reasonably convincing evidence that episodic, or at
least episodic-like, memory is involved.
In fact, “following the hippocampus” may be a way to explore the evolutionary origins
of episodic memory. The assumption would be that if a hippocampus is present, then
episodic memory, or important elements thereof, may also be present. Such a strategy
avoids the complicated behavioral methods necessary to identify episodic memory.
However, it is potentially problematic for exactly the same reason: It may be possible for
an animal to have a hippocampus without showing all the behavioral features of such a
memory.
Birds have a hippocampus, part of the paleocortex (ancient cortex), even though they do not
have a structure homologous to the mammalian neocortex (Clayton et al., 2003; Vargas,
Bingman, Portavella, & López, 2006). Even fish have a hippocampus, or more accurately, a
brain structure called the lateral pallium that is anatomically, genetically, and functionally
homologous to the avian and mammalian hippocampus (Vargas et al., 2006). Fish use it to
represent memory of the spatial environment, and it incorporates timing information
(Broglio et al., 2005; Murray, Wise, & Graham, 2018). Indeed, as we saw in Chapter 12, the
hippocampus is one site of grid cells that play an important role in representing environ-
mental locations even in bats, rodents, and humans. That is certainly episodic in that the cells
determine position and timing relative to the present environment, even though the en-
vironmental representation itself is built up over many different exposures and thus has
semantic qualities as well.
These observations suggest that key components of episodic memory originated by the
first appearance of bony fishes about 430 million years ago. However, whether these
components have always supported the kind of recollective experience we think of as epi-
sodic memory is doubtful. It will take a great deal of clever experimentation to determine
whether or not the episodic memory evident in gorillas, rats, and scrub jays shows continuity
over nearly 80% of the timespan of vertebrate evolution.
Also to be determined is the significance of discontinuities in the evolution of the hippo-
campus. Humans have a disproportionately large hippocampus compared to other primates,
and its posterior portion substantially enlarged relatively recently, i.e., during hominin
evolution. But, was this to support improvements in episodic memory, or alternatively, in
executive control or spatial ability? (Schilder, Petry, & Hof, 2019).
Semantic memory
How episodic memory gives way to semantic memory seems a bit mysterious. Logically,
every piece of knowledge that we possess began as an episode. For example, there was a
specific time and place that we first learned that 8 times 6 equals 48. At one time in our lives,
soon after our first exposure to that fact, we might well have remembered the specific cir-
cumstances under which we learned it, an indication of reliance on episodic memory. Now,
many years later, we do not. Somehow, multiple episodes have become something we simply
know to be true.
One possibility is that episodic memory is required for encoding into semantic memory, so
that in due course, multiple episodes build our knowledge structure. However, this does not
seem to be the case in that some amnesiacs have severely impaired episodic memory yet still
acquire new semantic memories (Rosenbaum et al., 2014; Verfaellie, Koseff, & Alexander,
2000). The alternate possibility, which appears more likely, is that the two memory systems
exist at least partially in parallel. Faulty operation of one would therefore not necessarily affect
the other. As we have seen, there is anatomical evidence for this view, with episodic memory
calling on the hippocampus and semantic memory on anterior temporal cortex.
Superficially, semantic memory should be much easier to demonstrate than episodic
memory, seeming to require only that information be recalled in a way that reflects some
understanding of meaning, and at a sufficient delay to represent long-term memory.
However, the situation is more complex than that, because conditioning also produces
behavior that appears meaning-laden. Thus, in the classic Pavlovian study, when a dog
salivates on hearing a bell, it appears that the dog understands the meaning of the bell: Meat is
coming. But does it? Remember that conditioning is a form of learning that is found in
flatworms and likely derives, at minimum, from the first emergence of neural nets
605 million years ago. A strengthening of simple neural connections through repeated
association seems more plausible than “understanding” at such an evolutionary remove.
One possible way around the conundrum may be to adopt an anatomical criterion.
Semantic memory involves the lateral temporal lobe, and thus its evolution might be revealed
by tracing the emergence of lateral temporal mechanisms of memory. Functional imaging
evidence suggests this may be a workable solution. Thus, while semantic memory involves
the lateral temporal lobe, conditioning involves widely scattered brain areas (Cabeza &
Nyberg, 2000), as might be expected from its arbitrary, associational nature.
Why would semantic memory draw on a specific region of the cortex such as the lateral
temporal lobe? Rogers et al. (2006) viewed the area as a hub that links modality-specific areas
of the brain. Thus, a semantic memory consists of a collection of facts linked together as a
concept. For example, a grapefruit has a waxy-feeling skin, is yellow, and emits a sour odor
as well as a satisfying squirting sound when dug into by a spoon. All of these features are
modality-specific – tactile, visual, olfactory, and auditory – and together comprise the
modality-free concept of a grapefruit. The lateral temporal lobe appears to be the cortical
region that links component features into an overall representation in semantic memory.
The use of lateral temporal cortex as a modality-free memory hub may have originated
in humans. There appears to be little evidence that macaques use the area in the same way.
To be sure, the tip of their temporal lobe – called the temporal pole – is involved in dis-
criminating between familiar and unfamiliar faces (Landi, Viswanathan, Serene, & Freiwald,
2021), and nearby perirhinal cortex (literally cortex “near the nose”) located in the medial
temporal lobe combines visual features in order to assign objects to classes (Bussey, Saksida, &
Murray, 2002). But because they are both visual, these operations are modality-specific.
One strong possibility is that the temporal pole and perirhinal cortex were the evolu-
tionary “kernels” of a semantic memory system that now primarily involves lateral cortex in
Memory 255
humans. Semantic dementia affects medial as well as lateral temporal areas (Landin-Romero
et al., 2016), although medial damage alone does not produce the full syndrome. For that,
lateral damage is required (Rogers et al., 2006). In humans, relative to monkeys and
chimpanzees, lateral temporal areas are greatly expanded in size and have become connected
to frontal lobe language areas, consistent with the input of meaning (semantic memory) into
language (Rilling et al., 2008).
However, it must be stressed that semantic memory is in part dependent on “local” levels
of the cortex where perceptual processes are conducted. Thus, damage to particular areas of
the brain can cause an inability to perceive particular classes of things. For example, fusiform
cortex lesions can affect face recognition (Iidaka, 2014), occipital lesions color recognition
(Bouvier & Engel, 2006), occipitotemporal lesions the recognition of living things
(Humphreys & Riddoch, 2003), superior temporal lesions music recognition (Sihvonen
et al., 2016), and so on. In a broad sense, such perceptual deficits can be viewed as semantic:
The meaning of a class of objects is lost because they cannot be recognized.
The lateral temporal cortex should therefore be viewed as only one level, although the
most general level, of a broader semantic memory system. The implication is that other
animals have the local elements of such a system even though they may lack the more general
component. Or, in evolutionary terms, human semantic memory may be much older in its
local levels than it is in its general one.
Conclusion
Truly comparative research in memory is surprisingly meager given that animals have
figured prominently as memory research subjects. Nevertheless, habituation, a decline in
response to repeated stimulation, can be regarded as a universal memory phenomenon,
with origins tracing to single-cell organisms. Association in the form of conditioning
is nearly as universal, extending at least as far back as the cnidarian divergence over
A case for universality, at least for vertebrates, can also be made for sensory memory.
Sensory memory is a short-lived trace that preserves much of the physical form of stimuli. It
lasts less than half a second up to ten seconds depending on the sensory modality. In the case
of human visual sensory memory, there is strong evidence of both a peripheral retinal
component and a central brain component, although in both cases the “icon” is best viewed
as an aftereffect of nervous system activity. Because other vertebrates have similar sensory
modalities and receptors, it is reasonable to believe they have the peripheral component of
sensory memory.
However, the universality assumption may not be valid in the case of the central com-
ponent, at least for the visual modality, because the brain area involved (V1) is a late
mammalian innovation dating to about 220 million years ago. Rhesus monkeys appear to
have the central component, as indicated by the existence of delayed masking.
Unfortunately, we do not have data on earlier-diverging taxa.
Comparative research is also sparse with respect to short-term memory, a small-capacity
form of memory that holds information for about 20 seconds in the absence of rehearsal.
Short-term memory capacity and search time are linked, such that fewer “slots” are
available for items requiring more memory, while search time is longer. Limited research
indicates that pigeons, monkeys, and humans all show evidence of a recency effect, in
which the most recently encoding items show increased recall, indicating the widespread
existence of short-term memory. However, its duration is haphazard across taxa, and it
appears that its neocortical mechanisms as found in primates are absent in birds. Thus,
primate and bird short-term memories appear to represent convergent evolution.
For the present, there is no evidence of intermediate memory in humans. It has been
found in birds and several invertebrates, with a measured duration on the order of one to six
hours depending on the species.
Long-term memory has been a more fruitful area for comparative study. Episodic
memory, which is memory for particular events, has been demonstrated in the lowland
gorilla King. King can reproduce the order of closely spaced events at intervals well beyond
the duration of short-term memory. His performance appears to demonstrate one-trial
learning of circumstances he knows are no longer true, that persist for a substantial length of
time, and that cannot be attributed to familiarity alone, together indicating the presence of
episodic memory.
Scrub jays and apes also exhibit episodic memory by searching for either of two types of
food cached in single events, contingent on delay which affects the integrity of the food.
Studies of rats likewise suggest the existence of episodic memory, and implicate the hip-
pocampus, the same anatomical substrate of episodic memory that is found in primates in-
cluding humans. Because all of these species, including birds, have a hippocampus, there may
well be a common evolutionary origin for episodic memory. However, it is unclear to what
extent it has supported a recollective quality of memory throughout its history.
Finally, semantic memory (memory for facts) may have had its origins in local brain areas
where particular classes of stimuli are recognized. If so, its history is likely to prove very
complicated, as each local area may have had a separate evolutionary trajectory. However,
the most general level of semantic memory may only have emerged in humans, involving
modality-free lateral temporal cortex mechanisms. It is possible that this was an outgrowth
of primate processing of multiple visual features in nearby perirhinal cortex as well as the
temporal pole.
15 Language
One day in 1995, a New York Times reporter visited a primate research facility in Georgia
and witnessed an interesting interaction. A bonobo named Panbanisha, walking with her
trainer Dr. Sue Savage-Rumbaugh, abruptly pressed three symbols on a portable keyboard,
multiple times in different orders. The symbols signified “Mad”, “Fight”, and “Austin”.
Savage-Rumbaugh surmised that there had been a fight at the residence of Austin, a
chimpanzee at the facility, which Panbanisha confirmed. Subsequently, it was discovered that
there had indeed been a fight between two chimpanzees over the use of computer equip-
ment. It had apparently been heard by Panbanisha in a different building some 200 feet
distant (Johnson, 1995).
Copious anecdotal evidence of a wide variety of cognitive skills in general and language
skills in particular have been provided by apes trained in the use of symbols or sign language.
From the Panbanisha anecdote, it seems straightforward to infer the existence of episodic
memory (recollection of a previous incident), semantic memory (identification of Austin
through sound alone), representational capacity (mapping the concept of Austin on to a
symbol), vocabulary (employment of a set of symbols to convey meaning), and syntax or
grammar (organization of symbols in orders that succeed in conveying meaning). To say that
studies of ape language have revolutionized our thinking about the mental capacities of our
nearest relatives would be an understatement.
But how much of the inferred mental repertoire of apes is based in science, and how much
in wishful thinking? As we have seen, there is reason to believe that apes do have episodic
memories. At minimum, they have elements of semantic memory in being able to assign
meaning to stimuli, even if they lack the most general, modality-free aspect of human se-
mantic memory. In this chapter, the remaining inferences from the Panbanisha anecdote are
examined, and we consider the extent to which apes show language capabilities in the form
of representational capacity, vocabulary, and grammar. We then consider how these capa-
cities led to human language, first considering evolutionary changes in the brain, and then the
chronology of changes – both physiological and behavioral – that created modern language.
Representational capacity
The ability to mentally represent the world in a realistic, literal way has been termed primary
representation. It refers to a direct semantic relationship between what is in the head and what
is in the environment (Leslie, 1987). Human infants show evidence of primary representation
from a very early age. By 4-1/2 months, they reach for suspended objects, indicating that
they use boundary information to separate objects from the surrounding environment. At this
age, infants appear to extract a considerable amount of information about objects, in that
distance, size, and movement all affect reaching. Even earlier, by six weeks of age, infants can
DOI: 10.4324/9781003137863-18
detect the difference between an object that is partially hidden behind a second object, and
one with the hidden part actually missing (Spelke, 1982).
Primary representation is clearly a prerequisite for language in that an object must be
mentally represented before it can be named. However, the ability to perceptually separate
objects from the environment, and even understand their meaning, is an ancient one and as
such sheds little light on language evolution. More complex representations, on the other
hand, yield more interesting relationships to language.
Secondary representation
Secondary representation refers to the ability to separate a primary representation from its en-
vironmental reference for hypothetical purposes (Suddendorf & Whiten, 2001). For example,
using a banana as a play telephone implies secondary representation because in the real world,
bananas are not telephones.
The relevance of secondary representation to language is that it allows names to be used
without their environmental references being present (Suddendorf & Whiten, 2001). Before
cell phones, it was common to say “I have a telephone in my office” without being in the
office, a displacement in space, or “I used to have a telephone”, a displacement in time, or “I
need to find a telephone”, a reference to the entire universe of telephones. The name could
even be used metaphorically, as in “I played telephone”, the child’s game in which state-
ments become progressively distorted as they are transmitted in a chain from one individual
to another.
Several phenomena indicate fairly strongly that apes are capable of secondary re-
presentation. As we have seen in previous chapters, chimpanzees can plan the creation of
tools, selecting an appropriate twig from which the leaves are stripped to become a “fishing”
tool, or a stick whose end is sharpened to become a spear. Secondary representation must be
present to allow the raw materials to be visualized as tools, which before their creation are not
literally present in the environment. It is also present when home-reared chimpanzees play
with dolls, bathing them or giving them something to “eat” (Tomasello & Call, 1997). Wild
chimpanzees, especially female ones, have been observed treating a log or stick as a baby, e.g.,
making a nest for it, or carrying it for periods of several hours (Kahlenberg & Wrangham,
2011).
The ape ability to perform hidden displacement tasks has also been interpreted as in-
dicating secondary representation. In one such task, an object is hidden in a small box, which
is then concealed in a larger box. The smaller box is then removed but no longer contains the
object. On discovering this absence, if test subjects look for the object in the larger box they
are considered to show secondary representation because the hidden object has been inferred
to have a hypothetical existence inside the larger box. Human one-year olds fail this test but
two-year olds typically pass. Chimpanzees, gorillas, and orangutans also pass (Collier-Baker,
Davis, Nielsen, & Suddendorf, 2006; Jaakkola, 2014; Suddendorf & Whiten, 2001).
Some of the most striking evidence of secondary representation comes from studies of
mirror-image recognition, in which apes demonstrate that they recognize themselves in a
mirror by using it to view parts of their body they otherwise cannot see. For example, many
chimpanzees will reach up to touch a mark placed on their brow, having used the mirror to
discover the mark (Anderson & Gallup, 2015). This is secondary representation because the
animal recognizes that the image is not itself an actual chimpanzee, but rather a hypothetical
chimpanzee representing them.
Is there evidence of secondary representation in more distant relatives of humans, such as
monkeys? Both New World and Old World monkeys generally fail hidden displacement
tasks, with their few apparent successes perhaps attributable to low-level strategies such as
Language 259
“pick the last-touched box” and not to secondary representation. The same may be true of
lesser apes (Jaakkola, 2014). Monkeys generally, including capuchins, squirrel monkeys,
macaques, and baboons, do not pass the mirror “mark” test, nor do lesser apes as a rule
(Anderson & Gallup, 2015). Thus, among primates, secondary representation appears to be
largely a great ape capacity.
Vocabulary
The creation of a secondary representation is basically the creation of a symbol. A banana is
not an actual telephone, but it can be a symbol of a telephone. Indeed, it has been argued that
even so simple a cognitive act as creating a mental image is symbolic, because the image is not
itself what it represents (Russon, 2004). In effect, some thing has been parsed from its en-
vironment, isolated, and given independent status as a mental entity.
Conceptually, it seems a small step to give such entities names and begin building a vo-
cabulary. Evolutionarily, however, it is a huge step mastered by only one living species and
dabbled in, with prodding, by a handful of others. A little thought gives some idea why the
step is so large. First, a concrete means of reference must become established, both to transmit
symbols and to receive them. Will the symbols be transmitted visually, e.g., through hand
gestures? Or will they be transmitted auditorily, e.g., through vocalizations? Also, how is
such a system bootstrapped from nothing, so that a symbol is both known by its transmitter to
be producible, and by its receiver to be meaningful? Finally, there must be sufficient mental
capacity on the part of both the transmitter and the receiver that multiple symbols can be
combined to convey actions and to flexibly cover new situations. For example, it might do
no good to tell hunters to “throw” if they are not sure when to throw, or what, or where.
Thus, communication is likely to be ineffective if both the transmitter and the receiver have
difficulty handling multiple symbols.
Of these varied parts of the larger problem, reception of symbols seems much the easiest to
achieve. A wide variety of species – including, it is safe to say, all primates – can readily learn
that one symbol represents a food reward and another does not. Discrimination learning has
been claimed to be a fundamental ability of all vertebrates (Moore, 2004). However, Russon
(2004) pointed out that the symbolic abilities of apes go well beyond mere associative
processes. For example, some chimpanzees understand how a scale model or photograph of a
room relates to its full-scale counterpart, and can use it to find a hidden soda. Others,
however, fail to master this task (Kuhlmeier, Boysen, & Mukobi, 1999). These results suggest
that as a species, chimpanzees are on the edge of understanding that a representation of a
space is symbolic of it, an ability acquired in humans’ third year of life (Russon, 2004).
Then, too, the use of multiple internalized symbols seems within the capabilities of
chimpanzees. For example, the idea of using a hammer to hit a nut placed on an anvil leveled
by a wedge represents a hierarchy in three levels, which chimpanzees routinely master. In
contrast monkeys have not demonstrated a capacity to hierarchically represent multiple levels
(Russon, 2004).
From the standpoint of great apes including hominins, therefore, the biggest problems in
establishing a vocabulary do not appear to be receiving or combining multiple symbols.
Instead, they are the establishment of a transmission system, and its bootstrapping so that the
transmitter knows the vocabulary is producible and the receiver knows its meaning.
Ape language studies

In ape language studies, both the establishment and bootstrapping of a transmission system are
neatly sidestepped. Human tutors provide the system (e.g., sign language) and a producible
vocabulary (e.g., individual signs) to teach meaning to the receivers. Given such substantial
intervention, the process cannot closely resemble how language initially emerged in hominin
prehistory. Nevertheless the outcomes are likely to be informative concerning early limits in
the growth and use of vocabulary.
How do scientists teach an ape to use sign language? First, they show the ape a sign in an
appropriate context, molding the animal’s hand to produce it. As they do this, they give a
reward. Over the next month, caretakers watch to see if the ape produces the sign. If two or
more caretakers see it used on at least 15 days of the month, it is concluded that the ape has
acquired it. In three years of such training, an average of 130 signs are learned regardless of
whether the learners are chimpanzees, gorillas, or orangutans (Blake, 2004).
Use of the signs is often spontaneous, and sometimes involves creative combinations such as
“eye drink” for contact lens solution, “candy drink” for watermelon, and “cookie rock” for a
stale Danish. Signs are also sometimes invented. Generalization often occurs when a specific
sign is not known: E.g., calling a cookie a cracker, a cow a dog, or using the sign for “open” to
request that water be turned on. As the Panbanisha anecdote at the beginning of the chapter
implies, and has been more formally observed, signs can be used to refer to things displaced in
time and space (Blake, 2004; Gardner & Gardner, 1998; Savage-Rumbaugh, McDonald,
Sevcik, Hopkins, & Rubert, 1986). However, in most cases, signs are used to request either
objects or actions, such as “flower” or “chase” (Rivas, 2005).
Panbanisha herself, of course, learned visual symbols called lexigrams rather than sign
language, which she used by pressing either a keyboard, touchscreen, or card-based array.
Panbanisha’s half-brother Kanzi learned lexigrams spontaneously without his arms being
placed in position and without reward. Both bonobos also consistently responded to human
speech as long as the words were in their vocabulary, e.g., with Kanzi reacting appropriately
to the request “Will you take some hamburger to Austin?” (Savage-Rumbaugh, 1992).
Some of these studies give an indication of the vocabulary size that can ultimately be
achieved by apes. Koko, a lowland gorilla, reportedly learned 600 signs in about 16 years, with
her ultimate acquisition projected to be up to 2,000 signs. However, the number of commonly
used ones was projected to asymptote at around 500 (Clark et al., 1990). Kanzi, the bonobo, has
been said to use somewhat less than 400 lexigrams (Paulson, 2007). However, these counts are
informal and may be inflated. In more formal, controlled counts, Kanzi and Panbanisha
averaged about 80% correct on tests using 256 lexigrams, suggesting a vocabulary size of about
200 (Lyn, 2007). Even so, it could be that fewer lexigrams or signs are commonly used. In a
count based on 22 hours of videotaped interactions, involving five chimpanzees, only 88
different signs were observed (Rivas, 2005). In comparison, there are approximately one
million English words, and human authors use a corpus numbered in the several to many
thousands – e.g., 7,000 in the case of Jane Austin and 20,000 in the case of James Joyce
(Macintyre, 2007). Educated adults have receptive vocabularies of about 20,000 base words and
may know several forms of each, such as “legal”, “legalese”, and “legalize” (Nation, 1993).
It seems clear that living apes, and by likely extension early hominins, are capable of
learning signs and symbols referring to objects, conspecifics, attributes, and actions. They also
appear to learn and use them appropriately to represent emotion, as in “mad”, “happy”,
“scared”, and “hurt”, although such uses are infrequent (Lyn & Savage-Rumbaugh, 2013).
Yet, with these capabilities come important limitations. Acquisition is slow even with
human intervention, between three and four symbols per month. In addition, while sign
combinations are frequently semantically meaningful, e.g., “drink coffee”, at least as fre-
quently they are not, e.g., “drink gum”. Longer combinations of three or four signs are also
repetitious about half the time, e.g., “flower gimme flower” (Rivas, 2005).
Nevertheless, it seems undeniable that an important kernel for the evolution of language is
present in our closest relatives. Even if utterances do largely represent requests (Rivas, 2005),
Language 261
communication is attempted. Indeed, it is reasonable to suppose that requests predominated
early in the history of human language.
But could an insipient language, once started, find a life of its own and be transmitted to
others, providing the bootstrapping necessary for the establishment of language? The answer
seems to be “yes” in apes. Kanzi learned his first lexigrams not through direct intervention,
but by casual observation of human attempts to teach them to his mother (Savage-
Rumbaugh et al., 1986). The chimpanzee Loulis learned about 50 signs from other chim-
panzees, although at a slow pace of a little less than one sign a month (Fouts, Fouts, & Van
Cantfort, 1989; Fouts, Jensvold, & Fouts, 2002). The implication is that the ape-human
common ancestor was probably capable of transmitting a small vocabulary-based language
system from individual to individual.
If transmission could occur, then the remaining major step in bootstrapping such a system
would have been the invention of the vocabulary itself. In the case of sign language, it is not
hard to imagine how that might occur. Some signs would very likely have started out as
natural communication gestures. A point might mean “that” or “there”, and a waving
gesture toward the body might mean “gimme” (Rivas, 2005).
Individual chimpanzees and lowland gorillas have been observed to develop repertoires of
about 10-to-30 natural communication gestures (Corballis, 2003), with several times that
number existing across a population (Roberts, Roberts, & Vick, 2014). Groups of orangutans
also have communication gestures numbered in the dozens (Cartmill & Byrne, 2010; Knox
et al., 2019). Having studied a community of wild chimpanzees in Uganda, Hobaiter and
Byrne (2017) identified 81 gestures. A small number of these were used to draw attention to
specific locations, perhaps modeling how environmental references came to be used in
language. Once received and acted appropriately upon, gestures could quickly have become
established as an initial vocabulary in an early hominin ancestor.
In apes, about half of gestures are manual in a broad sense of that term, i.e., involving the
hand, fingers, or arms. The remainder mostly involve body or head movement (Hobaiter &
Byrne, 2017; Knox et al., 2019; Roberts et al., 2014). In this regard, they differ from the
gestures of Old World monkeys, which overwhelmingly involve the body or head, and
cannot be construed as manual (Gupta & Sinha, 2019; Molesti, Meguerditchian, & Bourjade,
2020). Thus, a shift in apes away from body gestures to manual gestures may have been an
important step in the evolution of language.
Remarkably, comparison of the gestures used by one-to-two-year-old children with those
of chimpanzees reveals high overlap: About 90% of children’s gestures are also used by
chimps. Both also tend to produce gestures in pairs (Kersken, Gómez, Liszkowski, Soldati, &
Hobaiter, 2019). These observations raise the possibility that there are innate aspects of
gesturing derived from our shared ancestry. However, it is likely that at least some similarity
results from shared environmental contexts (Kersken et al., 2019). For example, an “em-
brace” gesture is stimulated by the presence of another individual, common to both human
and chimpanzee environments.
One difference between groups, however, lies in the use of gestures to refer to another
individual or an object. This is common in one-to-two-year-old humans but rare, though
present, in chimpanzees (Kersken et al., 2019). Thu while the study of toddlers suggests that
human and chimpanzee gestures derived from shared sources, toddlers seemingly come
equipped with refererential abilities that chimpanzees only minimally share.
Grammar
In my undergraduate classes, after describing some of the vocabulary-related findings of sign
and lexigram studies with apes, I ask my students to debate whether the capabilities reflect
language. Usually I get no takers on the “not language” side of the debate. Typically, every
student – or at least every student willing to express an opinion – endorses the conclusion that
apes can learn and use a rudimentary language.
But then, virtually all of my students are psychology students. To many psychologists
meaning is everything, or a big chunk of it. If a chimpanzee signs “give X” when “X”
is available, and the chimpanzee seems satisfied on receiving it, the intent for commu-
nication seems clear, the meaning definite, and the use of vocabulary in a language-like
way undeniable.
Linguists, in contrast, are often much more skeptical of the language nature of these
capabilities. To a linguist, the hallmark of language is grammar, not meaning. Grammar is
what allows speakers to communicate (and listeners to distinguish) the meaning of sen-
tences that use similar wording. For example, I might say, “The dog that the child is
chasing is wet”, or “The dog is chasing the child that is wet”. The two sentences use
identical words but have very different interpretations. Using grammar, we can generate
meanings that are not present in the vocabulary alone, greatly magnifying both the
complexity and subtlety of our communications.
On the grammar criterion, apes fall short. This first became apparent in the signing of the
chimpanzee Neam Chimpsky, “Nim” for short, playfully named after the famous linguist
Noam Chomsky. In his first four years, Nim learned 125 signs. Initial analysis of Nim’s two-
sign combinations showed some evidence for the consistent ordering that would be expected
if ape signing followed grammatical rules. For example, “more X” and “give X” combi-
nations outnumbered “X more” and “X give” combinations by nearly a 2:1 ratio. However,
this trend toward ordering broke down completely with combinations of three or more
signs, leading to the conclusion that grammatical rules were not present (Terrace, Petitto,
Sanders, & Bever, 1979).
Thus was ignited an academic controversy. On the pro-language side, Greenfield and
Savage-Rumbaugh (1991) produced data showing that Kanzi ordered lexigrams in a gram-
matical way. For example, two-sign combinations of action-agent (e.g., “carry person) and
action-object (e.g., “keepaway balloon”) outnumbered agent-action and object-action com-
binations by nearly a 6:1 ratio. Subsequent data from two bonobos, including Kanzi, and one
chimpanzee, confirmed frequent ordering preferences in two-lexigram combinations, and in
combinations of a lexigram with a gesture (Lyn, Greenfield, & Savage-Rumbaugh, 2011).
Furthermore, in the 1991 data, three-sign combinations of action-action-agent (e.g.,
“chase bite P”, where “P” was the designation of a human caretaker) outnumbered other
orderings by a 7:1 ratio. Unfortunately, however, this particular observation itself proved
problematic, as these were the only three-sign combinations sufficiently frequent to be
analyzable. Even then only eight instances had been observed among all combinations of
three or more signs, which themselves constituted only 10% of Kanzi’s corpus of 13,000
utterances (Greenfield & Savage-Rumbaugh, 1991).
In truth, the average length of ape utterances remains at about two vocabulary items, or a
little less, regardless of length of training (Lyn et al., 2011; Miles, 1990; also Terrace et al.,
1979, idealized data in Figure 15.1). This renders arguments over grammar rather sterile; it
may not make sense to argue whether grammar is observed in multiple-sign combinations,
when utterance length itself falls so short of human capabilities.
Clearly, apes have minimal access to complex grammatical structures. Nevertheless the
simpler trends in two-sign combinations may be important, particularly given parallels ob-
served in primate gesture and vocalization. In their natural gestures, chimpanzees commu-
nicate actions that also imply an actor, a simple two-element grammar (Fouts & Waters,
2003). With respect to vocalization, in both bonobos and common chimpanzees, a kind of
phonological syntax (ordering of meaningless sound elements) is observed in long-distance calls.
Language 263
Figure 15.1 Mean length of utterance over time, comparing Nim to three human children using oral lan-
guage. Nim remained “stuck” at fewer than two words per utterance, unlike human children.
For example, a “pant hoot” may be altered by inserting a “bark” into the sequence of
vocalizations. Such variations may be related to status, territoriality, and the need to maintain
contact with others (Ujhelyi, 1998). As in signing, and in natural gestures, they give a hint of
the beginnings of grammar. However, the grammatical structures are not complex.
The role of frontal brain areas

In contrast to apes using sign or lexigram forms of language, humans using language usually
vocalize. Nevertheless, our species shows some similarity to apes in how vocalization is
controlled. Specifically, regulation of the larynx in part involves area 6 in our frontal lobe (see
Figure 14.3). The same area constitutes the laryngeal motor cortex (LMC) in New World and
Old World monkeys, and in chimpanzees (Kumar, Croxson, & Simonyan, 2016; Simonyan,
2014).
Yet we also differ from other primates. While we do make some use of area 6, the primary
motor cortex (area 4) is more involved in vocal control, and these two areas taken together
comprise our LMC (Kumar et al., 2016; Simonyan, 2014).
Accompanying the anatomical distinction between species are differences in connectivity.
A major difference is that human LMC has vastly stronger connections than macaque LMC
with primary somatosensory cortex and the inferior parietal lobe. The strong connections
presumably exist to coordinate sensory feedback with phonemic information so that speech
can be adjusted on-the-fly by way of the LMC (Kumar et al., 2016).
Furthermore, connections of the LMC with laryngeal motoneurons in the brainstem are
direct in us, but indirect in monkeys. As a result, the LMC produces responses at the larynx
that are about three times faster in humans than in monkeys (Simonyan, 2014). That surely
was an important development in our evolution, as it enabled rapid, direct cortical control
over vocalization.
Broca’s area
Broca’s area, consisting of Brodmann areas 44 and 45, is another frontal area involved in
language. In Chapter 10 the roles of the area in human speech production and object
manipulationa were highlighted. Both actions have grammatical qualities, requiring the rule-
based sequencing of component movements. Brain lesions in the vicinity of Broca’s area
often result in agrammatism, the disordering of grammar. Thus, speech becomes telegraphic,
for example, with the intended sentence “Yesterday I went to the movies” possibly be-
coming “Yesterday go movie”. Also, the decoding of grammatically complex sentences fails.
For example, upon hearing the sentence, “The boy that the girl is chasing is tall”, agram-
matism patients are typically at a loss in judging which person is doing the chasing, and which
person is tall (Miceli, 1999).
Recent work suggests that area 44, comprising a portion of Broca’s area, is particularly
involved in the production of the complex phrase structures characteristic of natural human
language. When syntactical processing is complicated, the posterior temporal cortex is also
recruited by way of connecting tracts, especially the arcuate fasciculus. Arcuate fasciculus
connections are much stronger in humans than in other primates, potentially accounting for
the weak to nonexistent grammar of ape utterances. They are also more lateralized, to the left
hemisphere, in humans relative to chimpanzees and macaques (Balezeau et al., 2020; Eichert
et al., 2019).
As noted in Chapter 10, primate area F5 is homologous to the area 44 portion of Broca’s
area. F5 contains mirror cells that participate in the copying of sequential actions modeled by
others, implicating it in gesture. Furthermore in chimpanzees, asymmetry favoring the left
inferior frontal gyrus (the location of F5) correlates to the strength of right-handedness in
manual gestures, but not to handedness as evidenced in reaching (Hopkins & Cantalupo,
2004; Taglialatela, et al., 2006). Significantly, the correlation also extends to the insertion-
turning behaviors we examined in the handedness chapter (Hopkins, et al., 2017). Those
behaviors can be viewed as having a sequential, grammar-like structure (e.g., grasp an object,
insert it into an opening, turn it, and pull it toward oneself). Furthermore, a link to speech is
suggested by the fact that chimpanzee communication gestures are more right-handed when
accompanied by vocalization, than when emitted alone (Hopkins & Cantero, 2003; Hopkins
et al., 2005). Together these findings strongly suggest that in the chimpanzee, vocalization
and gesture are both at least partially controlled by F5 in the left hemisphere.
The implication is that the involvement in grammar of what in humans is Broca’s area has
roots tracing back to F5 in our common ancestor with chimpanzees. But should we attribute
the origin of those roots to gesture, or to vocalization? The answer is of critical importance,
because the difference is between a gestural origin or a vocal origin of human language.
On one hand, Taglialatela, Russell, Schaeffer, and Hopkins (2008) argued that lesioning
the Broca’s area homolog in monkeys does not affect their vocalizations. That observation
could be taken as supporting an early evolutionary role for the area specifically in gesture
rather than vocalization.
However, on the other hand, F5 in macaques activates during the production of lips-
macking, a form of vocalization (Shepherd & Freiwald, 2018). Furthermore, both macaques
and chimpanzees produce lip-smacks in a rhythm averaging four times a second – the same as
in human speech, reflecting the production of syllables with an open-closed mouth cycle
(Pereira, Kavanagh, Hobaiter, Slocombe, & Lameira, 2020). Together these results imply an
evolutionary continuity of F5/Broca’s area involvement in vocalization, dating back to or
prior to the divergence of Old World monkeys from our ancestral line.
In truth, the most likely scenario for the origin of language is that it was both gestural and
vocal. In comparison to using only one modality, using both improves signal detection,
disambiguates meaning, and increases the amount of information transmitted (Wilke et al.,
2017). Bonobos and common chimpanzees often pair gestures and vocalizations when
communicating, and pairing improves the chances of obtaining the desired end compared to
the use of either alone (Pollick & de Waal, 2007; Wilke et al., 2017). A further indication of
Language 265
Figure 15.2 Movement of the mouth and tongue accompanying the fine motor movements of a child.
Source: Wesley and his tongue, CC BY 2.0, Christopher Cornelius.
the intimate link between gesture and vocalization is that when chimpanzees make fine
motor movements with their hands, their mouths often make accompanying movements
(Wacewicz, Zywickzynski, & Orzechowski (2016). Human children, of course, do much the
same (Figure 15.2).
Interestingly, in contrast to common chimpanzees and bonobos, the pairing of vocalization
and gesture in gorillas and orangutans appears to be rare, even though each behavior alone is
fairly common (Knox et al., 2019; Poss, Kuhar, Stoinski, & Hopkins, 2006). This suggests
that coproduction of vocalizations and gestures may have originated, in large part, with the
chimpanzee-human common ancestor. Thus, it seems reasonable to suppose that at the very
beginning of human language, we made use of all of the communication tools at our disposal
in order to make ourselves understood. Gesturing and vocalization together were very likely
those tools.
The role of perisylvian brain areas

Producing vocalizations, of course, assumes that the intended recipients can decode the
sounds and understand their meaning. In this regard, perisylvian brain areas (areas located
around the Sylvian fissure, also called the lateral fissure, see Figure 15.3) are critically im-
portant in modern humans. The primary auditory area, where sound first enters the cortex, is
on the superior surface of the temporal lobe in Heschl’s gyrus. On the left side just posterior to
this in the superior temporal gyrus is Wernicke’s area, implicated in the decoding of speech
Figure 15.3 The Sylvian fissure in relation to Wernicke’s and Broca’s areas.
Source: Adaptation of Brain Surface Gyri.SVG, CC BY-SA 4.0, James.mcd.nz.
sounds. Above the Sylvian fissure is inferior parietal cortex, which is involved in the ongoing
storage of phonology (language phonetics), necessary to understanding connected speech.
The planum temporale

Comparative studies of the superior temporal areas involved in language have centered around
the planum temporale, or temporal plane, a small surface of cortex located lateral and posterior to
Heschl’s gyrus (Meisenzahl et al., 2002). This is generally held to contain secondary auditory
cortex as well as a portion of Wernicke’s area. Its main advantage as a unit of analysis is that,
unlike Wernicke’s area itself, it is anatomically easily definable and easily measured (although
there are slightly varying, competing definitions; see Meisenzahl et al., 2002).
Anatomical studies have shown that in humans, the planum temporale has a larger area in
the left hemisphere than in the right hemisphere (Gough et al., 2018; Meisenzahl et al.,
2002). In turn, planum temporale asymmetries, in area or volume, are found to correlate with
lateralization of language as assessed during anesthetization of each hemisphere in epilepsy
patients (Foundas, Leonard, Gilmore, Fennell, & Heilman, 1994; Oh & Koh, 2009). In the
larger of these studies, of patients with both asymmetric planums and asymmetric language,
45 of 46 with larger left planums had left hemisphere language, and 7 of 9 with larger right
planums had right hemisphere language, an impressively high agreement rate of 95% (Oh &
Koh, 2009). Others have indicated that the size of the planum temporale on one side or the
other correlates to language lateralization as assessed by brain imaging (Josse, Mazoyer,
Crivello, & Tzourio-Mazoyer, 2003; Tzourio-Mazoyer, Crivello, & Mazoyer, 2018).
Together these studies suggest that the area plays some role in language, and that left
hemisphere predominance in language is reflected in a larger left planum temporale.
The left-larger pattern is seen in about 65–80% of humans showing asymmetry in either
direction (Gough et al., 2018; Tzourio-Mazoyer et al., 2018). Thus, it is a matter of interest
that about 80% of tested great apes show it as well (e.g., Cantalupo, Pilcher, & Hopkins,
2003; Hopkins et al., 2016). The asymmetry appears to pertain to orangutans as it does with
the other great apes (Cantalupo et al., 2003), suggesting that it originated at least 15 million
years ago, although the number of tested animals is small.
Language 267
Analysis suggests that a similar asymmetry is found in macaques (Gannon, Kheck, & Hof,
2008) and baboons (Marie et al., 2018), potentially extending its evolutionary emergence
back at least 29 million years ago. Accompanying the anatomical asymmetry is a behavioral
one in which macaques hear “coo” and “scream” vocalizations better in the right ear than the
left, implicating the left hemisphere in their perception. Also, forward of the planum
termporale, cells located in the anterior left superior temporal gyrus selectively respond to
species-specific calls. To the extent that such calls constitute a kind of meaningful vocabulary,
there is a parallel to human language processing, which uses anterior portions of the gyrus
when recognizing words and phrases (Rauschecker, 2018).
Inferior parietal cortex

Above the Sylvian fissure, the human inferior parietal cortex is involved in phonological
coding and phonological working memory (Liebenthal, Sabri, Beardsley, Mangalathu-
Arumana, & Desai, 2013). Its anterior portions in particular are active in word rhyming
tasks (Kircher, Nagles, Kirner-Veselinovic, & Krach, 2011; Seghier et al., 2004). Intriguingly,
the anterior portions are also involved in comprehending and producing hand gestures
(Jax, Buxbaum, & Moll, 2006). It is therefore an area of particular interest if early language
was both gestural and vocal in nature.
The evolutionary history of the inferior parietal cortex is divided into two phases, an
initial one in which a left hemisphere size advantage was established, and a later one in
which the supramarginal and angular gyri first appeared. In modern humans a left hemi-
sphere size advantage is visible in terms of a Sylvian fissure that is longer in the left
hemisphere than in the right, especially in the portion posterior to the central sulcus (i.e.,
bordering the inferior parietal lobe). The asymmetry is also found in great apes, including
orangutans, and traces to an extended anterior portion of the left inferior parietal lobe
(Cantalupo, et al., 2003).
Could it have occurred even earlier than the orangutan divergence? Initial studies of
Sylvian fissure asymmetry in monkeys emphasized the lateral aspect of the fissure and pro-
duced inconsistent results (Heilbroner & Holloway, 1988). However, Hopkins and collea-
gues subsequently discovered that the leftward asymmetry is much more pronounced at
medial locations of the fissure, and that it exists for apes, Old World monkeys, and New
World monkeys about equally (Cantalupo et al., 2003; Hopkins, Pilcher, & MacGregor,
2000). Furthermore, it is the more medial asymmetry that is attributable to an extended
anterior parietal lobe (Cantalupo et al., 2003).
The initial phase of the evolution of inferior parietal cortex, therefore, seems to have
occurred prior to the New World monkey divergence, at least 44 million years ago. In all
likelihood the function of the area during this phase was concerned less with communication
than it was with reaching and with spatial attention, as in living monkeys (Battaglia-Mayer,
Mascaro, & Caminiti, 2007; Quraishi, Heider, & Siegel, 2007). These functions were sub-
sequently displaced away from the left inferior parietal lobe of modern humans, to more
dorsal parietal locations in the case of reaching, and toward the right hemisphere in the case of
spatial attention (see Chapter 12).
It is to the later phase of inferior parietal evolution that we must look for involvement in
early language. In Chapter 11, it was pointed out that the supramarginal and angular gyri,
comprising Brodmann areas 40 and 39, were human innovations that began with the genus
Homo (Tobias, 1995). They are not found in macaques at all (Figure 15.4). Homo habilis
endocasts show an accompanying feature not shared by australopithecines and apes: A
pronounced “rounded fullness” of the inferior parietal lobe (Tobias & Campbell, 1981). It is
this area that is involved in grasping independent of reaching, copying hand postures,
Figure 15.4 Human (top) and macaque (bottom) brains. Note that the inferior parietal cortex (PCi) of the
macaque lacks gyri present in the human.
Source: The RM was used in order to construct the connectivity matrices of the two species, CC BY-SA 4.0, A. Goulas,
M. Bastiani, G. Bezgin, H.B.M. Uylings, A. Roebroeck, et al.
phonological coding, and phonological working memory. Thus, the supramarginal gyrus
(area 40) plays a role in all of these (Frey et al., 2005; Jax et al., 2006; Liebenthal et al., 2013),
while the angular gyrus (area 39) aids the copying of hand postures by differentiating between
fingers and discriminating right from left (Denes, 1999). They are clearly structures one
might expect evolution to have altered if early language was both gestural and vocal in origin,
and evolution has done so.
Other temporal lobe areas

Finally, the role of other temporal lobe areas in language comprehension should be men-
tioned. In humans the middle and inferior temporal gyri are massively connected to the
region around and including Broca’s area. Again the arcuate fasciculus is responsible for much
of this, and the connections do not exist in similar magnitude in macaques and chimpanzees.
Furthermore, they are larger in the human left hemisphere than in the right hemisphere.
Their function appears to be to support lexical-semantic processing (Rilling, 2014). That of
course is consistent with the lateral temporal lobe’s role in semantic memory, as we saw in
Chapter 14.
Language 269
The hominin evolution of language: Language area changes
Thus far, the evidence argues for a joint gestural and vocal origin of language, with each
reinforcing the other. At the moment of the chimpanzee-human divergence, the human
ancestor very likely had chimpanzee-like capabilities. Those included a primary capacity to
mentally represent objects in the environment; a secondary representational capacity to refer
to them metaphorically or when they were otherwise not present; the ability to represent
objects with a small symbolic vocabulary of gestures and sounds, and to generalize, differ-
entiate, and combine their meanings; highly developed learning mechanisms that allowed the
transmission of vocabulary; and an ability to order, in a very basic way, at least two such
symbols.
Neurologically, area F5 and its surrounds in the frontal lobe had become specialized, by
virtue of mirror cells, in copying and sequencing actions modeled by others. The temporal
lobe was involved in recognizing vocalizations, and the region around the planum temporale
had long ago evolved the left-sided asymmetry that would serve as a substrate for further
language development. On the other side of the Sylvian fissure, the parietal cortex had long
been involved in mirror cell activity (Bonini, 2017), and the left inferior parietal cortex had
expanded.
Broca’s cap
Following on that beginning, it can probably be assumed that attaining speech-like utterances
depended at least in part on the conversion of F5 to more resemble the modern Broca’s area.
An indirect indicator of Broca’s area is Broca’s cap, an outward bulge of cortex in that vicinity.
It first appears with consistency in Homo habilis endocasts, having had variable expression in
apes and in australopithecines (Broadfield et al., 2001; Tobias & Campbell, 1981). Recently,
it was discovered that a well-defined Broca’s cap in endocasts counterintuitively depends on
the cap in the left hemisphere having shrunk relative to the corresponding area in the right
hemisphere, bringing its borders into better relief (Balzeau, Gilissen, Holloway, Prima, &
Grimaud-Hervé, 2014). Thus, if the cap is first clearly visible in Homo habilis, the shrinkage
may have begun by 2.4 million years ago. At about the same time, the gyri more directly
marking Broca’s area may have first made impressions on endocasts (Falk, 1983).
Falk (2014) reported that chimpanzees and humans have different sulcal patterns in the
region, affecting the positioning of Broca’s cap with respect to Brodmann areas.
Nevertheless, there were possible indications in an endocast of the 2-million-year-old species
Australopithecus sediba of a transitional state between chimpanzees and modern humans.
Recently, another study found that in 1.7-million-year-old hominins, the ventral end of the
precentral sulcus (see Figure 10.3) had shifted in a posterior direction, suggesting a late
expansion of inferior frontal cortex (Ponce de León et al., 2021). Taken together, these
results suggest reorganization of the region in hominins following the last chimpanzee-
human common ancestor.
Another discontinuity across species is apparent when the area of the third frontal con-
volution is measured as an approximation of Broca’s area, a quantity that can be assessed using
endocasts. In early hominins, the area was smaller in smaller brains, but beginning with late
Homo species (rhodensiensis/heidelbergensis, neanderthalensis, and sapiens), the size of Broca’s area
has been the same irrespective of brain size, even in relatively small-brained individuals
(Balzeau, et al., 2014). This seems reminiscent of the preservation of area 10 during the
dwarfing of the brain of Homo floresiensis, which was interpreted in Chapter 11 as suggesting
the area’s critical importance to that species. Thus, in completion of the analogy, Broca’s area
may have assumed critical functional significance by the onset of the later Homo species about
one million years ago.
By 370,000 years ago, according to a molecular clock estimate, an important genetic
change occurred that further enabled language. A gene known as FOXP2, located on
chromosome 7, has been linked to language capacity via an extended family with a de-
fective allele. Affected members of the family cannot properly combine component oral
movements such as protruding the tongue while closing the lips, and have trouble re-
peating even short word sequences (Lieberman, 2007). Imaging indicates that their Broca’s
area has reduced gray matter but increased activation, in the left hemisphere specifically
(Vargha-Khadem et al., 1998). The significance is that changes to the gene preceded the
split between Neanderthals and modern humans, although it postdated the chimpanzee-
human divergence. Thus, DNA analysis indicates that Neanderthals shared our form of
the gene (Krause et al., 2007), placing its origin somewhere in excess of 370,000 years
ago (Noonan, et al., 2006). To the extent that it is a “language gene” (a cautionary note
is that intelligence is affected as well; Lieberman, 2012), the result implies the existence of
language in that time frame.
Wernicke’s area
Although changes to Wernicke’s area in the temporal lobe are difficult to date, at some point
that area’s cellular microstructure changed. In chimpanzees, the cell bodies of neurons in the
planum temporale line up in minicolumns that are about 36 micrometers (0.036 millimeters)
wide in both hemispheres. In contrast, in humans there is a noticeable asymmetry, with
wider columns existing in the left hemisphere (50 micrometers) than in the right (43 mi-
crometers). Thus there appears to have been a “rewiring” of the planum temporale, pre-
sumably related to the left hemisphere comprehension of language (Buxhoeveden, Switala,
Litaker, Roy, & Casanova, 2001). Unfortunately, there is no evidence bearing on exactly
when this change occurred.
The hominin evolution of language: Peripheral changes

Alterations to anatomy in the periphery – i.e., the body and skull – were also necessary to
fully support language. One legacy of our primate past is an increase in larynx size relative to
the size of the body. The increase, seen with few exceptions in the full gamut of primates
from strepsirrhines through great apes, and thus extending back at least 68 million years,
lowered the pitch of vocalizations. In turn, that allowed them to project further in leafy
environments (Bowling et al., 2020). However, as we have seen, social primates also evolved
increased sensitivity to high-pitched sounds (Ramsier et al., 2012). Perhaps lower-pitched
vocalizations served to grab attention, while increased high frequency sensitivity permitted
better discrimination between vocalizations – a distinction that may apply to us today, as we
attempt to communicate in cluttered manmade environments.
A much more recent alteration to the vocal tract was a change in shape of the hyoid (a
horseshoe-shaped bone in the neck). About three million years ago Australopithecus africanus
had a bubble of bone upon its hyoid that is characteristic of chimpanzees and gorillas, but not
modern humans. The significance is that the bubble probably reflects the presence of air sacs
in the larynx (Alemseged, et al., 2006; Dunn, 2018). Much like increased larynx size, they
increased acoustic energy at low frequencies, allowing calls to extend further in forest and
woodland. However, simulations suggest that these effects make human speech sounds in-
distinct (de Boer, 2012). The implication is that australopithecine air sacs resulted in the
production of sounds more like ape vocal calls than modern human speech.
Language 271
When was this feature lost? Unfortunately, hyoids are not common among fossil assem-
blages. However, two exist from Homo heidelbergensis specimens dating to 530,000 years ago.
Both lack the bubble, and resemble the modern human hyoid (Martínez et al., 2008). Of
course, the loss of the bubble, and thus presumably the shift from vocal calls to more speech-
like utterances, could have occurred anytime in the 2.5 million years between the aus-
tralopithecine and heidelbergensis examples.
The range of speech sounds that could be uttered may also have increased with changes to
the face that began occurring between Homo habilis and Homo ergaster. Specifically, the face
began to flatten and the jaw to shorten. The tongue also shortened and reoriented, with the
result that it could produce greater leverage, increasing its flexibility and ability to articulate
sounds (MacLarnon & Hewitt, 2004).
The lungs
One substantial species distinction is that humans can control vocal air flow to a much
greater extent than apes. Our abilities are easily self-observed by monitoring breathing
while speaking out loud. Clearly, we can produce either sound bursts or continuous
vocalizations at will. This allows the sequencing of phonetic information, to the extent that
human sequencing of vocalizations can be ten times faster than that of apes (MacLarnon &
Hewitt, 2004).
An important element in the control of air flow is the control of breathing by the lungs
themselves. While speaking, exhalations become extended in time in order to produce the air
movement required for modification by the throat and mouth. Air pressure can also be
regulated by abdominal muscles controlling the lungs, to produce either loud or soft voca-
lizations. In contrast, other primates have much less control over breathing and cannot
produce vocalizations of anything like human complexity. In them, the regulation of vo-
calization much more involves the diaphragm that it does the abdominal muscles, the op-
posite of humans (MacLarnon & Hewitt, 2004).
Nevertheless in humans, some control over the breathing musculature is exerted by the
chest. It involves certain nerves exiting from the spinal cord at the thoracic vertebrae, those at
the level of the thorax. The nerves partially comprise the spinal cord, and so the vertebral canal
(the opening in the vertebrae through which the cord passes) must be wide enough to
accommodate them. This observation leads to a simple prediction: Species with the fine
breathing control needed for rapidly sequenced vocalizations should have enlarged vertebral
canals at the thoracic level, because of the increased size of nerves needed to control the
lungs. Of course, when looking for enlargement, it is necessary to take body size into
account, because larger species will have larger canals for that reason alone.
Putting this prediction to the test, MacLarnon and Hewitt showed that when thoracic
canal size is plotted against body size, all nonhuman primates track very closely to the
same line. In other words, when body weight is accounted for, they all have similar-sized
canals. However, modern humans place significantly above the line, indicating an en-
larged canal. Most critical to present purposes, though, were measurements of the size of
the thoracic canal in fossil hominin vertebrae. Neanderthals and early modern humans
likewise tracked above the primate line, while Australopithecus afarensis, Australopithecus
africanus, and a single Homo ergaster specimen fell almost exactly on it. The results strongly
suggest that precise control over breathing was achieved sometime between 1.6 million
years ago and 100,000 years ago, the age limits of the Homo ergaster specimen and the
more modern hominins. Unfortunately, at present we do not have sufficient vertebral
remains of intervening hominins to narrow this range further (MacLarnon & Hewitt,
1999, 2004).
The ear
A recent modeling of the auditory capabilities of reconstructed hominin ears suggests that
compared to modern humans, 430,000-year-old Homo heidelbergensis individuals had reduced
sensitivity in the 3,000–5,000 Hz range. That range is particularly important to the com-
prehension of speech generally, and consonants such as “t”, “f”, and “s” in particular. The
implication is that the structure of the ear changed at some point in our descent from hei-
delbergensis, to better accommodate the perception of modern speech sounds (Conde-
Valverde et al., 2021).
Strikingly, 130,000-year-old Neanderthals showed sensitivity in the 3,000–5,000 Hz range
that was nearly identical to modern humans. This result indicates that whatever occurred to
bring extended sensitivity to both species, operated sometime in the time window of 130,000
to 430,000 years ago (Conde-Valverde et al., 2021).
The jaw
Turning to the jaw, unlike Homo erectus we have a protruding, flat-surfaced chin, sometimes
described as an “inverted T” (Figure 15.5). Analysis of a series of jaws of modern Homo
sapiens, Neanderthals, and earlier specimens often attributed to Homo heidelbergensis, suggest
that it emerged about 90,000 years ago in modern humans (Schwartz & Tattersall, 2000).
However, that may only have been the final visible manifestation of a trend that began as
early as Australopithecus afarensis 3.7 million years ago, progressively pushing the chin forward
of the teeth (Pampush, Scott, Robinson, & Delezene, 2018).
The protruding chin has long been an evolutionary enigma, as its appearance does not
appear related to evolutionary changes in chewing. However, analysis of forces exerted by
Figure 15.5 A human chin with an “inverted T” (added for emphasis) formed from the mental protuberance
in the center, and the mental tubercle on each side.
Source: Adaptation of Sobo 1909 90.png, public domain, Dr. Johannes Sobotta.
Language 273
the tongue during speech do indicate that protruding chins reduce stress (Ichim, Kieser, &
Swain, 2007). Thus, its appearance about 90,000 years ago may be a sign of increased ar-
ticulatory ability. Whether that explanation can be stretched to a protrusion beginning as far
back as the australopithecines, of course, remains to be seen.
The vocal tract

A relatively late evolutionary change is the “verticalization” of the vocal tract (Figure 15.6).
At least as early as Homo heidelbergensis (530 kya), and as late as Neanderthals (30–200 kya), the
vocal cavities in adults were oriented more horizontally, as in apes, rather than vertically as in
modern humans (Lieberman, 2012; Martínez et al., 2013). While chimpanzees show some
verticalization during development, relative to humans it is not as great, and it does not
include the static descent of the hyoid into the throat that is found in human adults
(Nishimura, Mikami, Suzuki, & Matsuzawa, 2003; Nishimura, 2018).
Modeling the sounds that the more horizontal ape airway can produce suggests that vowels
would have had reduced intelligibility compared to modern speech (Lieberman, 2012; but
see Boë et al., 2019, for an opposing view). Indeed it appears that certain vowels, specifically
the vowel sounds in “ma”, “see”, and “do”, cannot be produced by nonhuman primates at
all (Lieberman, 2017). Brown and Golston (2006) have argued that evolving a vertical vocal
tract with a low larynx was also essential to produce a full range of consonants. Either way,
Figure 15.6 The “verticalization” of the modern human vocal tract, which is much more horizontal in apes,
Homo heidelbergensis, and Neanderthals.
Source: Adaptation of Midsagittal diagram unlabeled.svg, public domain, Wugapodes.
the full modern range of sounds would not have become possible until the vocal cavities
became fully vertical in modern Homo sapiens (Barney, Martelli, Serrurier, & Steele, 2012;
Lieberman, 2007). The date has been suggested as somewhere between 40,000 and
90,000 years ago (Lieberman, 2006). At the same time, the root of the tongue descended
deeper in the throat, becoming thicker and more rounded, and better able to control
air flow during vocalization (Lieberman, 2007).
Also consistent with change between Neanderthals and modern humans, is the finding that
genes influencing the development of our vocal tract – the vocal cords, pharynx, and larynx –
are overrepresented among genes that differ between the two species (Weiss et al., 2021).
Clearly something was working to favor the selection of more modern vocal tract char-
acteristics, and that something was no doubt language.
The hominin evolution of language: Behavioral changes

Some theorists have argued that language only developed rapidly with the proliferation of
tools and decorative artifacts some tens of thousands of years ago (e.g., d’Errico,
Henshilwood, Vanhaeren, & van Niekirk, 2005; Zilhão, 2007). In their eyes, the creation of
artifacts is a symbolic act that implies the use of language for purposes of representation and
instruction.
Proposing a link between language and the proliferation of artifacts does seem a leap of
faith, however. After all, it is not hard to imagine sufficiently intelligent but languageless
beings using spatial perceptual, memorial, and motor processes both to create artifacts and
to transmit knowledge of how they were created. If decorative artifacts are indicative of
language, then any decorative artifact of any age must be assumed to imply the existence
of language. In that case are we really willing to assume that language is implied by stone
tools decorated with red ochre, dating from over 160,000 years ago (Marean et al., 2007)?
Or by a shell etched with a geometric design, dating from about 500,000 years ago and
attributed to Homo erectus (Joordens et al., 2015)? It doesn’t seem unreasonable to require
additional evidence before drawing such conclusions.
“Proto-World” language
However, there is additional behavioral evidence – though highly controversial – of a de-
velopment in language on the tens-of-thousands-of-years scale. It emerges from the com-
parative study of languages, suggesting that all existing language families may partly derive
from an original language spoken about 45,000 years ago (Ruhlen, 1994b). Specifically,
tracing the common roots of words has led to a claimed convergence on a small vocabulary
reflective of a hunter-gatherer society, with words that mean “ashes”, “bone”, “dog”,
“earth”, “water”, and so on. A reconstruction of 27 of the original words has been proposed
(Ruhlen, 1994a). For example, “kuan” is taken to mean “dog” and is proposed as the root of
the word “hound” in English, while “aq’wa” is thought to mean “water” and is proposed as
the origin of the Latin and English word “aqua” (Bradshaw, 1997; Ruhlen, 1994a).
This hypothetical “Proto-World” language is quite controversial. Evidence of it has been
called subjective, poorly repeatable, and even unscientific (McMahon, 2004). Notable
problems are that apparent correspondences between languages can be coincidental, and that
words can not only be inherited from an earlier language, but can also be borrowed from
unrelated ones (Nettle, 1999). It also is not clear how a 45,000 year-old language would have
spread across the globe.
However, it is worth pointing out that the Proto-World hypothesis places something of an
upper limit on the emergence of modern language. If it is untrue, then modern languages
Language 275
have even more recent origins. Either way, it must be the case that earlier languages, as-
suming they existed, were less successful. The reason why that might be can only be a matter
of speculation. However, the 45,000 year old date roughly coincides with the lower date
limit on the verticalization of the vocal tract, suggesting that modern language may have
depended on evolving a novel capability to produce a wide range of sounds.
The evolutionary process

In this description of language evolution, the evolutionary process itself has received short
shrift. However, for the most part little need be said. Language has such clear adaptive
value, in its ability to recruit the help of others and in teaching the young and transmitting
culture, that it seems certain that once started, natural selection would ensure its con-
tinuance. The main caveat concerns whether the most recent elaborations of language
were too recent to have been much affected by natural selection (Box 15.1). Otherwise,
the universal nature of language is a testament to the power of evolutionary processes to
produce profound change.
Box 15.1 Did reading evolve?
Writing systems date back only about 5,500 years, yet reading is a nearly universal
human capability. The short time frame in which reading emerged, and its rapid
spread, imply that it is not a direct product of natural selection.
Instead, reading must have emerged as a co-option of other capabilities. Dehaene
and Cohen (2007) have suggested that one of the brain sites involved in reading
occupies an intersection of cortical areas sensitive to object identity and foveal
stimulation. The implication is that this visual word form area (VWFA), in or near the
occipito-temporal sulcus, is located where it is because recognizing words presented
visually calls for sensitivity to particular objects (words) at a particular location (the
fovea). In other words, reading has co-opted preexisting capabilities, and a preexisting
cortical map, for new purposes.
Even so, however, co-option requires the preexisting circuitry to be altered during
development. Consistent with this, the predominant role of the left hemisphere in
reading does not emerge until several years after reading begins. Thus visual field
studies of word recognition show no visual field difference – and therefore no
hemispheric difference – from the beginning of reading at about age 5 to around ages 8
to 10, when a transition to increasing left hemisphere representation begins. By age 11,
the leftward shift is complete ( Boles, et al., 2008). Similarly, reading-related evoked
potentials also shift leftward during development as reading finds its “optimal location”
in the left ventral visual system ( Dehaene and Cohen, 2007). Presumably it is optimal
because other language processes are located in the left hemisphere as well.
A second reading-relevant location is the left angular gyrus (Brodmann area 39),
involved in recoding visual words into phonological forms ( Boles, 2002; Pugh et al.,
2000). The angular gyrus adjoins Wernicke’s area, yet how “left hemisphered” an
individual is in reading, fails to positively predict how left hemisphered that individual
is in recognizing auditory language. In fact, there is actually a slight negative
relationship between the two, so that a person with an especially strong left hemisphere
involvement in one tends to have a reduced left hemisphere involvement in the other
( Boles, 1998). This pattern is consistent with the co-option view: The more left
parieto-temporal cortex is co-opted by either reading or auditory language compre-
hension, the less is available for the other.
It may be more appropriate to ask, “Will reading evolve?” Given its importance to
education and economic security, and the impact those have on reproduction, the
answer is almost certainly “yes”. However, as with natural selection more generally,
there is no way to predict the time frame or the precise nature of future adaptations.
Conclusion
Language did not spring forward in one great leap, like Athena from the forehead of her
father Zeus in Greek mythology. Instead it followed the course of other complex abilities,
starting crudely and acquiring increased sophistication by degrees over many millions of years
(Table 15.1). It was prefigured by the increased larynx size of primates over 68 million years
ago, and by the appearance of frontal lobe mirror cells prior to the Old World monkey
divergence 29 million years ago. These assisted the copying of others’ actions, an operation
that would later prove critically important in learning communication gestures.
Table 15.1 Milestones in the evolution of language. Mya = millions of years ago
Date Achievement Examples/notes
Bef 68 mya Change in larynx size In primates: Increased size relative to size of
the body.
Bef 29 mya Frontal lobe mirror cells In living monkeys: Activity during grasping,
etc., and observations of same by others.
Asymmetric planum temporale In living monkeys: Larger on the left side.
Superior temporal gyrus involvement In living monkeys: Greater left-side
in recognizing vocalizations involvement.
Inferior parietal cortex asymmetry In living monkeys: Longer Sylvian fissure
on the left, indicating a larger left side.
Four times per second vocal rhythm In living monkeys: Lip-smacking. In
humans: Syllables.
Bef 15 mya Secondary representation In living apes: Tool manufacture; hidden
(displacements and metaphors) displacement; mirror-image recognition.
Symbolic capacity In living apes: Play objects; hierarchical
planning; learning of externally provided
languages (signs and lexigrams).
Simple grammar In living apes: Tendency to order two-
element sequences in externally provided
languages and in natural gestures;
vocalization insertions.
A “vocabulary” of natural In individual living apes: Repertoires of
communication gestures 10–30 gestures.
Shift from mostly body and head In living apes: Mostly manual (hand, finger,
gestures and arm) gestures
~12 mya Skilled handedness, possibly In living gorillas and chimps: Population
indicating left hemisphere area F5 right-handedness in tube task,
development hammering.
Bef 7.5 mya F5 co-production of communication In living chimps: Activation of F5 during
gestures and vocalizations co-occurrence of right-handed
communication gestures and
vocalizations; mouth movements
accompanying fine hand movements.
(Continued)
Language 277
Table 15.1 (Continued)
Date Achievement Examples/notes
Aft 7.5 mya Increased laryngeal motor control In hominins: Laryngeal motor cortex
(otherwise recruitment of area 4, with stronger
uncertain) parietal connections and direct
connections to the brainstem.
Increased connections between In hominins: Relative to chimps.
Broca’s area and the temporal lobe,
especially on the left
Asymmetric minicolumns in In hominins: Found in humans but not
Wernicke’s area chimps.
Aft 3 mya Loss of air sacs, allowing speech-like In hominins: Hyoid bones suggest air sacs
vocalizations in Australopithecus africanus 3 mya, not
in Homo heidelbergensis 0.5 mya
2.4 mya Appearance of a well-defined Broca’s In hominins: First found in Homo habilis.
cap and gyri marking Broca’s area
(homologous to F5)
Appearance of supramarginal and In hominins: First found in Homo habilis.
angular gyri; “rounded fullness”
of inferior parietal lobe
~1.9 mya Face flattening and jaw shortening In hominins: Occurred between Homo
noticeable; shortening and habilis and Homo ergaster.
reorienting of tongue
~1 mya Stabilization of size of Broca’s area In hominins: Size of third frontal
convolution stabilized beginning with
Homo heidelbergensis.
0.1–1.6 mya Increased breathing control In hominins: Enlarged thoracic vertebral
canal.
Bef 0.37 mya FOXP2 allele affecting Broca’s area In hominins: Shared by Neanderthals and
Homo sapiens.
Bef 0.13 mya Increased sensitivity to speech In hominins: In the 3000–5000 Hz range,
frequencies shared by Neanderthals and Homo sapiens.
~.09 mya Protruding, flat-surfaced chin In hominins: First appeared in modern
supporting speech stresses humans as the culmination of a trend
beginning 3.7 mya.
.04–.09 mya Selection of modern vocal tract; In hominins: Verticalization and
full range of vocalizations overrepresentation of the vocal tract in
gene changes in modern humans.
.045 mya Appearance of modern vocabulary?
However, new cognitive components would also be necessary. Secondary representational

capacity, appearing sometime prior to the orangutan-human common ancestor 15 million
years ago, allowed understanding of displacements in time and space. It also provided mental
stand-ins that could be dealt with metaphorically in place of actual objects. Mirror-image
recognition became possible too, with an image standing independently as a metaphorical
representation of the self. The importance of this capacity cannot be overestimated, because
the units of language – gestures and words – would need to be understood as metaphorical
references and not as objects in and of themselves. Thus was born a symbolic capacity.
A small “vocabulary” of natural communication gestures likely provided the first true grist
for the language evolution mill. Dozens of gestures are found in living orangutans, gorillas,
and chimpanzees. Thus a natural gestural “vocabulary” dates back beyond 15 million years
ago, as does a shift from mostly body and head gestures to manual ones. However, a fuller
exploitation of gestures probably depended on developments in frontal lobe area F5, dating
back about 12 million years ago as evidenced by population right-handedness in gorillas and
chimpanzees performing skilled tasks. This was a marker for the F5 ability to sequence motor
acts including gestures – another critical necessity in the evolution of language.
Before 7.5 million years ago, a Rubicon was reached: In the chimp-human common
ancestor, and possibly not before, F5 could co-produce communication gestures and voca-
lizations. Now two communication modalities could be mutually reinforcing, allowing
disambiguation of messages that might be obscured in only one. Sometime after three million
years ago, the loss of air sacs made speech-like vocalizations possible.
By the appearance of Homo habilis 2.4 million years ago, F5 had evolved into a discernible
Broca’s area, appearing as a notable protrusion (Broca’s cap) and as gyri known from the
traces of endocast sulci. Possibly at this time language of a crude, limited type was being
produced, perhaps both gestural and vocal in nature. To accommodate it, the inferior parietal
lobe developed its “rounded fullness”, as well as the supramarginal and angular gyri, pre-
sumably playing something like its modern role in comprehending gestures and speech
sounds. It may have been at this point, though the dating is uncertain, that minicolumn
asymmetry appeared in Wernicke’s area in the temporal lobe, and the arcuate fasciculus
increased in size and connections to improve transmissions between Wernicke’s area and
Broca’s area.
The remaining hominin language adaptations all appear to have had the function of al-
lowing more precise and discriminable vocalizations, so that after this point language became
heavily dominated by speech as opposed to gesture. Face flattening and jaw shortening in-
creased, and the tongue began shortening and reorienting. Sensitivity increased to the
3,000–5,000 Hz frequencies used in speech, As early as 1.6 million years ago, but certainly by
100,000 years ago, the thoracic vertebral canal enlarged to pass nerves to the chest that
allowed increased breathing control during speech. Before 370,000 years ago, the FOXP2
gene mutated, affecting the development of Broca’s area and presumably profoundly influ-
encing speech.
The increased mechanical stress of speech-related oral movement resulted in selection of a
protruding, flat-surfaced chin by about 90,000 years ago, and around that time, or perhaps as
late as 40,000 years ago, the vocal tract became vertical, supporting a full range of vocali-
zations including a full set of consonants and discriminable vowels. By 45,000 years ago, a
modern vocabulary may have emerged, which some believe has left its imprint on all of
today’s language families.
Thus, language has at least a 68-million-year background, divided into roughly four
periods. In the first period, larynx size increased, and the foundational capacities of imitation,
secondary representation, symbolism, and a natural vocabulary of communication gestures,
emerged in monkeys and ancestral apes. The second period, dating from perhaps 15 million
years ago to shortly before 7.5 million years ago, saw an increasing specialization of area F5 in
producing skilled motor acts, to the point that it could co-produce gestural and vocal
communications. By the end of the third period about two million years ago, F5 had become
Broca’s area, and the inferior parietal lobe had further developed. Crude, limited speech may
have been produced and understood. Finally, in the fourth period, from about 1.9 million
years ago to about 40,000 years ago, there were a number of adaptations of the face, jaw,
tongue, vocal tract, and chest nerves that resulted in more discriminable speech and perhaps
at the end of the period, the beginning of modern vocabulary.
16 Consciousness
Our human cognitive nature produces a number of complex behaviors such as tool-making
and language. However, in the opinion of many, a nonbehavior, consciousness, is the
supreme achievement of the human mind.
Daniel Dennett (1981) likened the popular view of consciousness to an “inner light” that is
either on or off, and that is obvious from the inside. The problem, Dennett noted, is iden-
tifying consciousness from the outside. Are animals conscious? Could a machine be conscious?
Now, we must define external criteria that denote consciousness.
Dennett’s description, however, only scratches the surface of the mystery. Many psy-
chologists closely identify consciousness with attention, taking the view that whatever we are
attending to, we must be conscious of (e.g., Posner, 1978). However, that assumes a unitary
nature of attention that may not exist. Attention can be split between information sources
(Scharlau, 2004) and according to some theories, between tasks (Boles & Dillard, 2015). But,
are we really splitting consciousness when we split attention?
Even so, attention is only a beginning point in the universe of thought about con-
sciousness. In ever-expanding circles, consciousness has been equated with intellect
(Ornstein, 1972), the sum total of cognitive processes (Titchener, 1909), matter (Miller,
1962), reality (Eccles, 1966), and even unity with God (White, 1974). Some have linked it to
quantum physics (Mukhopadhyay, 2014). Small wonder, then, that others have argued that
consciousness cannot be defined (Granit, 1977).
The approach taken in this chapter is to examine behaviors that have been interpreted as
implying consciousness. This is a functional approach to the topic, emphasizing what
consciousness brings to behavior. Even so, some readers will demur. Thus, while sup-
porting functional approaches, Allen and Bekoff (2007) noted that some philosophers
consider consciousness an epiphenomenon of other mental processes, itself having no effect
on behavior.
It is likely that some of the behaviors that have been interpreted as implying consciousness
will be viewed as more compelling than others. But perhaps somewhere in the darkness, we
can catch a glimpse of the “inner light”.
Sensory awareness
An initial function of consciousness to consider is that of sensory awareness, the subjective
experience that we have sensed something external to us. At first glance, this may seem too
simplistic and self-evident to lend value to evolutionary analyses. However, certain failures of
sensory awareness in fact prove informative.
DOI: 10.4324/9781003137863-19
Blindsight and deaf hearing
Blindsight is a phenomenon in which an observer claims to be blind, yet shows unexpected
residual visual abilities. It results from partial or complete destruction of the primary visual
cortex (area 17; see Figures 16.1 and 10.4), producing blindness for part or all of visual space.
The basic demonstration of blindsight begins with the presentation of a visual stimulus in the
blinded area, to which the patient fails to respond. On prompting, the patient states that they
are blind and see nothing. However, if they are asked to point toward the place where the
stimulus was shown, they often are able to do so with surprising accuracy. Some patients can
even make discriminations of shape (e.g., squares from rectangles), identify line drawings of
animals or other objects, or discriminate colors, while simultaneously stating that they are
guessing (Ajina & Bridge, 2017; Trevethan, Sahraie, & Weiskrantz, 2007).
A similar phenomenon, deaf hearing, likewise occurs due to destruction of the primary
sensory cortex, this time Heschl’s gyrus or Brodmann area 41 bilaterally (see Figures 10.4
and 16.2). The patient denies hearing anything, but nevertheless orients to loud sounds like
hands clapping or fingers snapping (Garde & Cowey, 2000).
Blindsight and deaf hearing demonstrate that while sensory information entering the
brain through the primary cortex routinely reaches consciousness, when that route is
blocked it does not. The major visual route is the geniculostriate route, which proceeds from
the eye to the lateral geniculate nucleus to the primary visual cortex (area 17). It is this
route that produces visual awareness and is disrupted in blindsight. However, there is an
alternate tectopulvinar pathway that proceeds from the eye to the superior colliculus, then to
the pulvinar (a nucleus in the thalamus), and finally to the secondary visual areas of the
cortex (see Figure 16.1). This route bypasses area 17 altogether, providing cortical visual
input in the absence of area 17 function.
Is it the tectopulvinar pathway that supports the residual capabilities of blindsight?
Though long thought so, confirmatory evidence only emerged relatively recently. Leh,
Mullen, and Ptito (2006) studied hemispherectomy patients in which an entire cerebral
hemisphere had been surgically removed, producing profound blindness in one visual field.
They found that responses to visual stimuli in the sighted field were speeded by the re-
dundant presentation of the same stimuli in the blind field, a demonstration of blindsight.
However, the speeding of responses only occurred if the redundant stimuli were achro-
matic (i.e., in shades of white, gray, and black) and thus visible to the medium- and long-
wavelength cones that have inputs into the superior colliculus. If they were in colors
distinguishable only to short-wavelength cones, which have no input into the superior
colliculus, no speeding occurred. A subsequent fMRI study reported activation of visual
cortex beyond V1 and V2, when the redundant stimulus was achromatic but not when it
Figure 16.1 The geniculostriate and tectopulvinar visual pathways to the cortex.
Consciousness 281
Figure 16.2 The auditory pathways to the cortex.

could be seen only by short-wavelength cones (Leh, Ptito, Schönwiesner, Chakravarty, &
Mullen, 2010). Together these results argue strongly that the intact pathway in blindsight is
routed through the superior colliculus, as is true of the tectopulvinar pathway. This route,
of course, does not appear to provide visual awareness.
In the auditory modality the major pathway is from the ear to the inferior colliculus, and
then to the ventral portion of the medial geniculate nucleus, before ending up in Brodmann
area 41, the primary auditory cortex (see Figure 16.2). Destruction of area 41 on both sides
can result in the deaf hearing phenomenon. The apparent cause is a secondary pathway
leading from the inferior colliculus to the dorsal portion of the medial geniculate nucleus,
then bypassing area 41 before ending up in secondary auditory cortex (area 42). No auditory
awareness appears possible through this route, although as indicated, the patient orients to
loud sounds (Garde & Cowey, 2000).
What can blindsight and deaf hearing tell us about the neural substrate of consciousness?
On one hand, it seems clear that under normal circumstances, stimulation of primary cortex is
a prerequisite for sensory awareness. If such stimulation doesn’t occur as in blindsight and deaf
hearing, sensory awareness does not occur. The most obvious possibility, then, is that stimu-
lation of primary cortex directly generates awareness. However, this can quickly be rejected on
the basis of a study of macaques by Nakamura and Mishkin (1980). They surgically isolated
visual cortex in one hemisphere – striate, inferotemporal, and other higher visual areas – from all
other cortexes in that hemisphere. They also blinded the other hemisphere by disconnecting
optic nerve input to it, and they disconnected the hemispheres by severing the cerebral com-
missures. The result was behavioral blindness. The monkeys could not perform a previously
trained visual discrimination, bumped into objects, and failed to react to fear-inducing objects.
In other words, even though the visual system seemed to be fully intact in one hemisphere –
though disconnected from the rest of the cortex – the monkeys showed no evidence of visual
awareness. Awareness therefore is not a property of visual cortical stimulation alone.
A second possibility is that information from the primary cortex travels to some other brain
structure that itself produces awareness. While this is difficult to rule out – a definitive test
would require ruling out all other brain structures, one by one – it seems unlikely. That’s
because in blindsight and deaf hearing, the residual sensory capabilities enter the cortex in
secondary areas just barely removed from the primary cortex. It seems very likely that they
have access to all the brain structures that primary cortex can access, yet awareness does not
result. Note that this also means the secondary areas, taken alone, do not produce awareness.
If primary and secondary sensory areas are not alone responsible for consciousness, what is?
There appears to be something unique about primary cortex in interaction with other areas of
the brain that results in awareness.
The role of reentry
A promising idea is that neurologically speaking, reentrant connections support such inter-
actions. In other words, the primary cortex stimulates higher-order cortical sites that in turn
send connections back to primary cortex. Perhaps that is somehow what results in sensory
awareness (Lamme, 2003; Rees & Frith, 2007).
There is in fact direct experimental evidence that supports the role of reentry. When
Transcranial Magnetic Stimulation (TMS) to V1 is used to evoke an experience of phosphenes
(imaginary points of light) in intact brains, awareness of the phosphenes can be prevented
by V1 restimulation at a lower intensity that does not itself generate phosphenes, 30 msec or
so after the initial stimulation (Pascual-Leone & Walsh, 2001). This strongly suggests that if
reentry is prevented using subthreshold TMS, there is no awareness. Delayed TMS has also
been found to degrade V1 function compared to no delay, again consistent with reentry
although any effects on subjective awareness were not examined (Camprodon, Zohary,
Brodbeck, & Pascual-Leone, 2010).
Of course, the reentry solution does not completely resolve the problem, for we still have
little idea how it is that reentry results in sensory awareness (Lamme, 2003). In particular we
have little understanding how we generate the ineffable sensory qualities that baffle even the
most dedicated introspective observers (e.g., why is yellow yellow, or sour sour?). However,
reentry does at least allow us to begin an evolutionary analysis of the origins of sensory
awareness, by tracing the history of reentrant connections.
In this regard, reentrant connections into V1 certainly exist in macaques, where they have
been most extensively studied (Hupé et al., 2001). They also exist in squirrel monkeys, a
New World species (Rockland & Knutson, 2000), as well as in rats (Johnson & Burkhalter,
1996), ferrets, and cats (Cantone, Xiao, McFarlane, & Levitt, 2005). Indeed, feedback
connections are a fundamental characteristic of the mammalian brain (Johnson & Burkhalter,
1996). Thus, their evolutionary history dates as far back as the origin of mammals about
However, it is not clear whether they have supported sensory awareness across that entire
time span. Although cats have residual visual abilities following destruction of primary visual
cortex (Payne, Lomber, MacNeil, & Cornwell, 1996), which are consistent with blindsight,
we do not know whether the animals experience reduced visual awareness. What we do
know, however, is that monkeys experience blindsight, while simultaneously believing
themselves blind. Thus, Cowey and colleagues have found that macaques can localize stimuli
in their blind field. Yet if the same stimuli are shown in the same blind field, and the choice is
whether or not a stimulus was presented, the monkeys choose to respond that none appeared
(Cowey & Alexander, 2012). Thus, the monkeys appear to inform us that they believe
themselves blind. Monkeys can also be trained to respond to the location of stimuli in a blind
area even though they do not spontaneously shift their eyes to them (Moore, Rodman,
Repp, & Gross, 1995). These performances are very similar to those of human blindsight
patients who deny that a stimulus is present but who can localize it when encouraged to.
Putting these observations together it seems clear that sensory awareness dates back at least
to the human-macaque common ancestor about 29 million years ago. It may date back to the
origin of mammals 220 million years ago, if reentrant connections from higher to lower brain
areas are diagnostic of sensory awareness.
Attention
William James is widely credited with establishing a close correspondence between attention
and consciousness. In his book, Psychology (1892), he maintained that attention accentuates
Consciousness 283
and emphasizes perceptions that become the objects of consciousness, and that it ignores
(and thus causes consciousness to ignore) the rest of the many stimuli that constantly besiege
us. Later, authors equated consciousness with awareness and likewise emphasized the role of
attention in creating it (Posner, 1978; Taylor & Fragopanagos, 2007).
Problems with attention as consciousness

However, at least two issues arise with using attention as a proxy for the existence of
consciousness. The first is whether attention even implies consciousness. It can be argued
that any selection of one of multiple stimuli or stimulus attributes impinging on the
nervous system of an organism is a form of selective attention, yet this capacity is so basic
that it undoubtedly exists in all animals with nervous systems. Thus, chickens can make use
of spatial cues to attend to a location, while ignoring other locational cues, and zebra fish
can quickly reverse their “attentional set” if a previously unrewarded color suddenly be-
comes rewarded (Krauzlis, Bogadhi, Herman, & Bollimunta, 2018). Without the ability to
select stimuli or attributes significant to survival, and to ignore unimportant ones, an
animal’s chances of survival and propagation would be compromised. Thus, selection
should be (and presumably is) a universal nervous system characteristic, but we should
hesitate before claiming that the existence of a nervous system necessarily implies the
existence of consciousness.
A second issue with using attention as a proxy for consciousness is that attention is not a
unitary concept. Posner (1992) identified three distinct components. First, there is a se-
lective attention component, which for spatial selection at least depends on the parietal
lobe, primarily but not exclusively in the right hemisphere. Second, there is a component
that recognizes the meaningfulness of stimulation, and that involves anterior cingulate
cortex. Third, there is an alertness component, maintaining wakefulness and readiness to
respond to stimulation, that is dependent on a right frontal mechanism. All of these
components also involve subcortical areas such as the thalamus.
But which component should we identify with the existence of consciousness? The
selective component is what William James had in mind, but we also habitually speak of
being conscious (awake) versus unconscious (asleep), roughly corresponding to Posner’s
third component. Most of us should have no problem viewing his second component as
consciousness-related too. Thus, if we receive a stimulus that suddenly provokes a re-
cognition of meaning, we often say that the meaning has become conscious. But if we accept
that all three represent consciousness, we not only make the task of identifying consciousness
in animals a much harder proposition, we open the possibility that a particular animal might
be conscious in some ways but not others.
Unfortunately, there is also no consensus as to what neural structures support con-
sciousness. Posner’s work appears to implicate attentional roles for the frontal and parietal
lobes, and for the cingulate cortex, but Lamme (2003) suggested that attention plays only a
supporting role in consciousness. He argued that while we are conscious of many things,
attention is merely what allows us to report one of those things, and that consciousness itself
results from recurrent interactions between sensory areas and widespread areas of cortex
(frontal, prefrontal, parietal, and temporal), that brings information into register with needs,
goals, and context. Merker (2007) has even questioned whether consciousness depends on
the thalamic-cortical connections involved in attention. He noted that children with hy-
droanencephaly, lacking a cortex but not in a persistent vegetative state, show indications of
consciousness by reacting to environmental events.
Also, troubling are the results of studies using TMS. In humans, TMS applied to the
parietal cortex disrupts both selective attention, and consciousness as defined as the ability to
report stimuli – but with no correlation across participants in the sizes of these disruptions
(Babiloni et al., 2007). The result suggests that the relationship between attention and
consciousness is at best a loose one.
Historically, the relationship between attention and consciousness has been an important
one. However, the issues surrounding how best to conceptualize that relationship and how to
relate it to behaviors or to neural structures whose evolution can be traced, appear too
fraught at present to take us far in using attention to trace the evolution of consciousness.
Metacognition
One possible function of consciousness is that it permits metacognition, the awareness of one’s
own cognitive states and processes. For example, it might involve a judgment of how much
one knows in a particular circumstance. This aids decision making by distinguishing between
situations where action can be taken because knowledge is sufficient, and situations where it
should be withheld because knowledge is insufficient. Such “feelings-of-knowing” are vague
and error-prone, as are other products of metacognition like judgments of how easily one
will learn something, or of the quality of one’s retrieved answers (Nelson, 1996). They can
therefore be viewed as a type of “fringe consciousness” that is constructed from the outcomes
of unconscious processes (Norman, 2017).
Even young children have metacognitive skills. In one study, picture-number pairs such as
a dog and the number “2” were presented for learning. Then in the testing phase, a number
was presented and the child could either choose to decline answering, or to view an array
of pictures with the aim of choosing the correct partner – e.g., the dog if a “2” had been
presented. If correct, a highly rewarding visual display was shown. If incorrect none was
shown, while declining to respond received a less rewarding display. The results showed that
4.5- to 5-year-old children declined to respond to pictures that were difficult to remember
40% of the time, but those that were easy to remember only 21% of the time. However
younger children, 4–4.5 years old, did not do this (34% versus 33%). The implication is that
“feeling of knowing” is a metacognitive faculty that develops beginning at about 4.5 years of
age (Liu, Su, Xu, & Pei, 2018).
In a second study, children always responded by trying to pick out a studied picture from a
larger array, but could indicate afterward whether or not they felt confident in their decision.
Children age 4–5 showed much higher accuracy when they felt confident than when they
did not (82% versus 28%), a difference that wasn’t found in children age 3–4 (56% versus
46%, a nonsignificant difference). Thus, the “confidence in retrieved answers” form of
metacognition (Nelson, 1996) appears to begin developing around age 4 (Liu et al., 2018).
Monkeys, too, show evidence of metacognition. Shields and colleagues tested two
rhesus macaques on their confidence in retrieved answers. A rectangle that was filled either
densely or sparsely with pixels was presented, and the task was to respond by pressing an
“X” to a dense rectangle or “O” to a sparse one. Difficulty was varied by changing the
density within each of these categories. Thus a dense rectangle could be relatively sparse,
or a sparse rectangle relatively dense, with either of these representing a difficult trial. After
learning the task, the monkeys were next introduced to confidence ratings, learning to
press a blue bar if they had confidence in their just-made response or a pink bar if not.
Food rewards and time-out punishments were arranged to appropriately incentivize the
monkeys. It was found that accuracy was higher when the monkeys expressed confidence
in their judgment that when they did not, by 14%. This was quite similar to the outcome
of a parallel experiment using adult humans, also finding a 14% differential (Shields, Smith,
Guttmannova, & Washburn, 2005). The outcome was also similar to that from a later study
testing event order judgments in macaques, showing that when the animals were allowed
Consciousness 285
to select which trials to respond to, accuracy was higher than when selection was not
allowed (Templer, Brown, & Hampton, 2018).
Are New World monkeys also aware of what they know? Tests administering a version of
the sparsity task to capuchins produced ambiguous results. Monkeys were allowed to make
an opt-out response when presented with the rectangle, with the expectation that they
would make the response more frequently in the most difficult trials. Five monkeys com-
pletely failed to do so in spite of appropriate incentives. However, a sixth monkey did so after
extensive experience with the task (Beran, Smith, Coutinho, Couchman, & Boomer, 2009).
A later set of studies used the opt-out procedure with a different discrimination task
involving picking the largest of a set of squares. Macaques were found to regularly use the
opt-out response, reaching 40% of the most difficult trials. Capuchins were much less likely
to use it, opting out of only 10% of the most difficult trials. A second experiment shrunk this
difference between species but did not eliminate it (Beran, Perdue, & Smith, 2014).
Other studies using varying methods have supported the existence of metacognition in all
of the great ape species (including humans) and in Old World monkeys (i.e., macaques).
Evidence for it is mixed in New World monkeys (i.e., capuchins), with some studies failing
to find it, and others finding either reduced proficiency or proficiency only in some in-
dividuals and not others (Beran et al., 2014). While including other monkey species in future
research would be desirable, the tentative conclusion is that New World monkeys are “on
the cusp” with respect to metacognitive abilities – and thus on the cusp with respect to
“fringe consciousness” as well. Thus metacognition may have barely begun to evolve in our
common ancestor with New World monkeys 44 million years ago.
Self-recognition
Another possible function of consciousness is that it allows self-recognition. Gordon
Gallup (1968) first reported self-directed behaviors in a chimpanzee following brief
exposure to a mirror:
The chimp’s initial responses to the mirror consisted of the typical other-directed
behaviors such as lip smacking, vigorous head bobbing, a few threats, and intense
inspection of the mirror image. [Afterward,] however, the other-directed orientation
was abruptly displaced…. He was observed to stick out his tongue at the mirror, and
shake his brass neck tag in front of the mirror. Perhaps the most significant evidence of
self-directed behavior was the fact that the chimp would actively groom various parts of
his body otherwise not visually accessible except in the presence of a mirror (for
example, the forehead and eyebrows).
Humans, of course, have no problem recognizing themselves in mirrors. Nevertheless, at

this point in his research, Gallup interpreted self-directed behaviors in animals less in terms
of higher-order cognition than in terms of conditioning. The mirror, he suggested, might
disrupt the stimulus-response pairings governing social interactions, and lead to the
learning of new contingencies between what the mirror shows and movement of the body
(Gallup, 1968).
All of that would soon change. By 1970 Gallup was able to report the consequences of
placing a mirror with each of four chimpanzees. The initial responses were as if directed to
another animal. However, around the third day, self-directed behaviors came to the fore.
Subsequently, and most importantly, after the chimps were anesthetized and a red dye was
applied to their eyebrow ridge and ear, they almost immediately began touching the affected
areas on reexposure to the mirror. The dye could be seen by them only in the mirror, so
clearly they used it to perceive and explore the markings. That in turn implied that they
understood the image was of themselves. In contrast, four macaques showed no self-directed
behaviors with similar treatment, even after prolonged exposure to the mirror. Based on this
difference between species, Gallup abandoned the conditioning explanation, arguing instead
that mirror self-recognition requires advanced intellect. Indeed, he indicated, it implies “a
concept of self” (Gallup, 1970).
In 1977, consciousness entered the argument. Gallup noted that the research of others
found no evidence of self-recognition in spider monkeys, capuchins, baboons, and gibbons
among other primate species (Gallup, 1977). This led him to conclude:
The unique feature of mirror-image stimulation is that the identity of the observer and
his reflection in a mirror are necessarily one and the same. The capacity to correctly infer
the identity of the reflection must, therefore, presuppose an already existent identity on
the part of the organism making this inference. Without an identity of your own it
would be impossible to recognize yourself. And therein may lie the basic difference
between monkeys and great apes. The monkey’s inability to recognize himself may be
due to the absence of a sufficiently well-integrated self-concept.
In other words, chimpanzees, who unlike monkeys can self-recognize, have a self-concept and
are thus self-aware. Furthermore, Gallup argued, self-awareness implies self-consciousness.
Individual differences in self-recognition

Subsequently Gallup and his colleagues reported on a long-term study of chimpanzee self-
recognition that revealed individual differences. A retesting of 12 animals first examined
eight years previously showed that most individuals who could self-recognize earlier,
continued to self-recognize (N = 6), and most that could not self-recognize earlier
continued not to (N = 2). However, others showed an unmistakable decline in self-
recognition with age (N = 4 individuals age 18–24 years). Thus, not all of the chimpanzees
had ever been able to self-recognize, and there was an age-related decline in the ability
among those that could (de Veer, Gallup, Theall, van den Bos, & Povinelli, 2003).
The aging effect confirmed the result of an earlier study, using cross-sectional design,
finding that while 75% of adolescent and young adult chimpanzees could self-recognize,
only 26% of older ones could (Povinelli, Rulf, Landau, & Bierschwale, 1993). In the words
of the authors, there appeared to be “a precipitous decline” beginning at 16–20 years of
age. On the other end of the lifespan, there were indications that mirror self-recognition
may not begin in chimpanzees until four to five years of age (Custance & Bard, 1994;
Povinelli et al., 1993), in contrast to beginning at one and a half to two years of age in most
human children (Schulman & Kaplowitz, 1977). Another important finding of the study
by Povinelli et al. was that the “mark test” of self-recognition sometimes gave results that
were incongruent with observations of other self-directed behaviors in a mirror. Thus
some animals failed to touch the red dye, yet manipulated their genitals or lips using the
mirror (Povinelli et al., 1993).
A number of these observations suggest that chimpanzees are on the evolutionary cusp of
self-recognition – and thus potentially of consciousness. Many, but by no means all, pass the
mark test. Some who fail the mark test nevertheless can use mirrors for self-inspection and
self-manipulation. Mirror self-recognition follows a developmental timecourse longer than
that of human children. It is also vulnerable to the effects of aging. In each case, these
conclusions suggest that chimpanzees are not far over an evolutionary divide between species
that can or can not self-recognize.
Consciousness 287
Self-recognizing species
So what species can self-recognize? Several orangutans have passed the mark test (Swartz,
Sarauw, & Evans, 1999). Gorillas were the subject of early controversy that has been resolved
in favor of self-recognition including passage of the mark test (Posada & Colell, 2007; Swartz
et al., 1999). Finally, common chimpanzees have been the most extensively studied species in
this regard, with 42 of 97 animals (43%) having passed the mark test as of 1999 (Swartz et al.,
1999). It is unclear whether there is any significant variation across great ape species in ability
to pass the test, because sample sizes have been small, and there has been insufficient sys-
tematic control over such variables as the age of the subject. Nevertheless, all great ape species
appear capable of self-recognition.
Among lesser apes, gibbons use mirrors to examine parts of their bodies, but they fail the
mark test (Hyatt, 1998; Ujhelyi, Merker, Buk, & Geissmann, 2000). One human-reared
siamang, however, passed it (Ujhelyi et al., 2000).
On the other hand, Old World monkeys such as macaques and baboons generally fail the
test (Gallup, 1970, 1977). Gallup reported leaving mirrors with macaques for periods up to
17 years without ever eliciting self-recognition, although the monkeys could use the mirrors
to orient to a person entering their room (Gallup, 1998). Attempts to shape the behavior of
macaques to produce self-touching of mirrored marks have had more success (Chang, Fang,
Zhang, Poo, & Gong, 2015; Thompson & Boatright-Horowitz, 1994). However, it is un-
clear whether success following conditioning has the same meaning as spontaneous self-
touching (Anderson & Gallup, 2015; Gallup, 1982). Thus, while Chang et al. (2015) were
able to rule out the possibility that conditioned self-touching of a dye mark was stimulated by
a mark on any monkey’s face, it seems possible that monkeys learned to self-touch in response
to a particular face, i.e., their own, without really recognizing that the face represented them.
On the other hand, Boccia (1994) reported that one of 14 pigtail macaques did pass the
mark test even without training, first wiping at the mark and then inspecting the hand.
Because this was such a rare and transient response, she suggested that the behavior be
considered “incipient recognition or protorecognition rather than as full self-recognition”
(Boccia, 1994, p. 358).
Another indication that some self-recognition may be present in macaques comes from a
study in which rhesus monkeys were fitted with electrode implants for other studies. The
implants used highly conspicuous blue acrylic blocks, and the monkeys used mirrors to in-
spect them. The monkeys then also used the mirrors to inspect body parts such as the genitals
(Rajala, Reininger, Lancaster, & Populin, 2010). However, in interpreting the results of this
study, it should be kept in mind that Gallup’s original aim was to use marks that could not be
felt or smelled (Gallup, 1970). This aim was not met in the case of the implants, which
certainly afforded tactile if not olfactory stimulation.
With respect to New World species, Gallup indicated that spider monkeys and squirrel
monkeys fail the test. Capuchins were also reported to consistently fail the mark test (Gallup,
1977, 1982; Roma et al., 2007). Yet subsequent research has found that they treat mirror
images differently than they do views of strangers of their species. While found in both sexes,
the effect is clearest in females, who show greater eye contact and less anxiety in the mirror
condition (de Waal, Dindo, Freeman, & Hall, 2005). It seems possible, therefore, that while
New World species are not generally capable of self-recognition, some notice that something
is “different” about mirror images.
The results appear to indicate that true mirror self-recognition, performed on a strictly
visual basis, exists among primates only in apes, and possibly only in great apes. Lesser apes and
macaques may show partial signs of self-recognition that depend greatly on the individual or
on conspicuous, multimodal stimuli. It may be that providing a tactile stimulus such as an
implant can cause a macaque to recognize a relationship between a mirror image and its own
body, without triggering true self-recognition.
Several other unrelated species have also been found to pass the mark test. A possible
encephalization effect is suggested by reports that dolphins and elephants do so. Reiss and
colleagues have found that bottlenose dolphins engage in self-directed behaviors while
viewing their marked bodies in mirrors. For example, they stretch the neck upward when
marked under the chin, or orient a marked side toward the mirror (Morrison & Reiss, 2018;
Reiss & Marino, 2001). Of course, this may not be the quite the same thing as self-touching,
for as we have seen it is possible for an animal to use a mirror to inspect body parts while
failing the mark test.
For their part, Asian elephants were initially reported to fail the mark test (Povinelli, 1989).
However, in that study the mirror was small and out of reach. Plotnik, de Waal, and Reiss
(2006) tested three Asian elephants using a larger, accessible mirror and found that one
passed. The others failed but nevertheless used the mirror for self-inspection.
The limitations of encephalization as a self-recognition predictor, however, are revealed
by a report that horses also pass the mark test (Baragli, Scopa, Maglieri, & Palagi, 2021).
Of 14 horses, three consistently acted aggressively or fearfully in response to a mirror. The
remaining 11 all showed greater reaction to marks placed on the cheeks than to invisible
marks, for example by scratching against a limb or fence. Yet horses are not highly
encephalized, having moderately large brains accompanied by large bodies.
Whether the mark test is passed by corvids, the bird family that includes crows, ravens,
jays, magpies, and jackdaws among others, has been controversial. An initial study by Prior,
Schwarz, and Güntürkün (2008) found that some individual Eurasian magpies attempted to
use their beaks, and succeeded in using their feet, to remove yellow marks visible only in a
mirror. However, negative results have been reported from the same species (Soler,
Colmenero, Pérez-Contreras, & Peralta-Sánchez, 2020), as well as from other corvids in-
cluding jackdaws (Soler, Pérez-Contreras, & Peralta-Sánchez, 2014), carrion and hooded
crows (Vanhooland, Bugnyar, & Massen, 2020), scrub jays (Clary, Stow, Vernouillet, &
Kelly, 2019), and azure-winged magpies (Wang et al., 2020).
On the positive side among corvids, the majority of house crows have been found to pass
the mirror test (Buniyaadi, Taufique, & Kumar, 2020). The Clark’s nutcracker has also been
reported to pass – although oddly, it more clearly did so when a blurry rather than a regular
mirror was used (Clary & Kelly, 2016). Overall, with respect to corvids, the results must be
regarded as mixed.
Two recent investigations of mirror self-recognition in fish have similarly resulted in
mixed and controversial results. Cichlids showed only aggressive responses to marked self-
images, that habituated over time (Hotta, Komiyama, & Kohda, 2018). Cleaner wrasses,
however, transitioned from aggressive reactions to their mirror image, to body orienting
toward the image, to scraping on the substrate in apparent attempts to remove the mark.
They did not show these behaviors when a nonvisible (transparent) mark was used instead
(Kohda et al., 2019). While these behaviors seem to indicate self-recognition, de Waal
(2019) has pointed out that the injection procedure used to create the marks was irritating
(a point conceded by the researchers), and that it may have served to draw visual
attention to the marks that would not otherwise have occurred. As de Waal stated, to pass
the mark test, “it is as if these animals need multimodal stimulation”. Apes need visual
stimulation alone. However, it seems fair to point out that this is only a plausible
interpretation of the results. The critical experiment using nonirritating marks has not
been performed, so it remains possible that visual stimulation alone would produce
self-recognition behaviors.
Consciousness 289
The role of encephalization
The diversity of species showing self-recognition – the great apes, Asian elephants, horses,
and possibly siamangs, dolphins, corvids, and cleaner wrasses – poses a challenge for phy-
logenetic interpretations. However, there is a sufficient correlation to encephalization to raise
the question of whether self-recognition emerges out of raw brain power. As we have seen,
great apes including humans have the highest encephalization quotients of all primates.
Siamangs are also rather high, though no more so than nonself-recognizing gibbons,
baboons, and spider monkeys (see Table 11.1).
Extending an encephalization analysis to mammals outside the primate order is proble-
matic, because as we have seen (Chapter 5) the power function exponent that best relates
brain size to body size in primates, is not the same exponent that best fits mammals in general.
Nevertheless, if we replace the 0.28 primate exponent with a 0.67 mammalian exponent, the
results are instructive as long as we recognize that it produces disordered results within
primates. What the results show is that Asian elephants have a relatively high encephalization
quotient, extending into the range of apes. Bottlenose dolphins have a quotient even above
that. Horses, however, show genuinely modest encephalization (Table 16.1).
What about corvids? Attempting to include members of a different order along with
mammals in an encephalization analysis is truly dicey, especially when there is evidence of
greater neural density in bird brains than in the brains of mammals generally and of primates
specifically (Olkowicz et al., 2016). However, it is possible to place magpies relative to other
birds. Based on the tabled brain volumes and body weights of nearly 1500 bird species
(Iwaniuk & Nelson, 2003, Appendix A1), a best-fitting exponent of 0.57 may be calculated.
In turn, applying that in an EQ equation places magpies at the 92nd percentile. That is
certainly a high value, although it is not truly exceptional in that 8% of the tabled bird species
have higher EQs. About half of those higher are of the family Psittacidae (parrots), an eighth
Table 16.1 Encephalization values for mammals including

elephants, based on a 0.67 exponent
Species EQ
pig 0.27
sheep 0.54
horse 0.73
rat 0.84
European cat 1.14
fox squirrel 1.43
ring-tailed lemur 1.45
gorilla 1.54
African elephant 1.67
Asian elephant 2.14
chimpanzee 2.32
bottlenose dolphin 3.93
human 7.51
Notes: EQ = brain mass/(0.12 ∗ body mass0.67), with masses measured

in grams. All values except horses and bottlenose dolphins from
Shoshani et al. (2006). Horse EQ calculated from adult brain and
body sizes provided by Cozzi, Povinelli, Ballarin, & Granato (2014);
dolphin EQ from sizes provided by Lefebvre, Marino, Sol, Lemieux-
Lefebvre, and Arshad (2006). These values cannot be directly com-
pared to EQ values cited elsewhere in the book, because of the use
of a different exponent as well as a multiplier in the divisor.
are of the family Cacatuidae (cockatoos) and another eighth are fellow corvids (family
Corvidae). Many of the higher-ranked species have a reputation for intelligence, so it might
be supposed that they are candidates for self-recognition. However, observation of Goffin’s
cockatoos (EQ percentile unknown) and keas (a species of parrot; EQ exceeding the 99th
percentile!) indicates they do not pass the mark test (van Buuren, Auersperg, Gajdon,
Tebbich, & von Bayern, 2019).
These results seem generally consistent with an encephalization effect on self-recognition.
However, the relationship is by no means perfect, either in mammals or birds.
The fact that encephalization bears some relationship to self-recognition, but an im-
perfect one, raises the possibility that self-recognition is the product of specific brain
mechanisms that tend to emerge with larger brains. In this regard, Hecht, Mahovetz,
Preuss, and Hopkins (2017) considered the possibility that it depends on the evolution of
connections between the parietal lobes and prefrontal cortex. Images of the tracts between
these areas revealed variations between individual chimpanzees, with some having a
prefrontal extension of connections and others not. Critically, those with the prefrontal
extension were more likely to pass the mark test. Success on the mark test was also related
to asymmetry in the connections, specifically a rightward asymmetry in the connecting
tracts and in connections to the Broca’s area homolog in chimpanzees. The researchers
concluded that mirror self-recognition depends on connections between parietal and
frontal areas that process body imaging and motor commands. By their interpretation
successful self-recognition depends on understanding, via mirror images, the correspon-
dence between commands to move and the resulting body movements. Some chimpanzees
seem to have the brain connections to achieve this and some not.
Whether posterior-anterior brain connections are related to self-recognition in other
species remains to be seen. Nevertheless, the observations that mirror self-recognition is most
prevalent among the great apes, but may have precursors in mirror-based self-inspection in
gibbons and macaques and in perceiving “something different” about mirror images in ca-
puchins, strongly suggest a long-evolving capacity among primates. If self-recognition reflects
consciousness, then consciousness may have evolved over many millions of years as well.
The role of sociality

A different explanation of mirror self-recognition was tested by Krachen, Lurz, Mahovetz,
and Hopkins (2019). They proposed that self-recognition actually has a social purpose: By
allowing introspections about one’s own mental states and experiences, similar states and
experiences can be attributed to others. Among other things this permits empathy. If so,
then mirror self-recognition should be related to other social abilities such as imitation and
perspective-taking, and unrelated to nonsocial cognitive tasks such as tool use and un-
derstanding causality. In general this prediction was borne out in a group of common
chimpanzees that numbered up to 82 depending on the test. Individuals who were better
self-recognizers tended to have greater social ability, but not greater nonsocial cognitive
ability (Krachen et al., 2019).
Although this outcome is promising, social explanations of mirror self-recognition may
have limited applicability. Orangutans, which are much less social than chimpanzees, can
nevertheless self-recognize (Swartz et al., 1999). On the other hand, macaques are highly
social but generally cannot (Gallup, 1998). Thus the ape-versus-monkey difference trans-
cends sociality, perhaps again pointing to encephalization and the evolution of specific brain
mechanisms of self-recognition. Of course, some version of all taken together might be true:
E.g., encephalization may have led to the evolution of specific brain mechanisms that led to
self-recognition that in turn supported social abilities in apes.
Consciousness 291
Theory of mind
As originally formulated, the term theory of mind referred to a proposed ability of chim-
panzees to impute the existence of mental states in themselves and others (Premack &
Woodruff, 1978). Though conceptually similar to metacognition, which involves assessing
the status of task-related mental processes, theory of mind is considered a separate ability
because it involves assessing states rather than processes, e.g., desires, thoughts, and beliefs
(Papaleontiou-Louca, 2008).
Gallup, Anderson, and Shillito (2002) asserted that having a theory of mind depends on
self-awareness, for without it, there is no basis for imagining the mental states of others.
This position predicts that animals that have no self-awareness as assessed by the mark
test, should also have no theory of mind. However, the relationship may not be so clear-
cut. For example, a basic theory of mind might be inferred from the ability to follow the
gaze of others, which indicates knowledge that others may be viewing something im-
portant. Yet gaze following is an ability that extends across many different species in-
cluding ones in which there is no evidence of self-awareness. For example, members of
some lemur species, representatives of the earliest-branching primate group, the strep-
sirrhines, follow one another’s gaze toward humans, food sources, and other lemurs
(Ruiz, Gómez, Roeder, & Byrne, 2009; Sandel, MacLean, & Hare, 2011; Shepherd &
Platt, 2008).
Gaze following has also been reported in ravens (Bugnyar, Stöwe, & Heinrich, 2004),
dolphins (Tschudin, Call, Dunbar, Harris, & van der Elst, 2001), dogs (Call, Bräuer,
Kaminski, & Tomasello, 2003), and goats (Kaminski, Riedel, Call, & Tomasello, 2005). It
should not be surprising then, that among primates, gaze following occurs not just among
lemurs but also among mangabeys and macaques (Drayton & Santos, 2017; Tomasello, Call,
& Hare, 1998) and all great apes (Bräuer, Call, & Tomasello, 2005; Kano & Call, 2014).
Skepticism that gaze following denotes a theory of mind has been expressed by Povinelli
and Bering (2003). In their view, the ability is one among many that are associated with
highly social species – deception, holding grudges, and organized hunting being others – that
emerge far in advance of the ability to interpret mental states. Simpler attentional, motiva-
tional, perceptual, and other abilities were regarded by Povinelli and Bering as underlying
gaze following in animals.
This could be a valid point if gaze following was as simple as merely shifting the eyes in
response to eye shifts in others. Even simple stimulus-response association could account for
the behavior since shifting is likely to lead to more positive outcomes than not shifting.
However, Tomasello and colleagues found that chimpanzees will effortfully approach and
look around barriers in order to see what human observers are gazing at (Tomasello, Hare, &
Agnetta, 1999), an observation that seems resistant to a simple stimulus-response association
explanation.
That chimpanzees understand something about what others see comes from research on
food competition. When a subordinate has the opportunity to view food hidden from a
dominant individual, the subordinate selectively retrieves that food rather than food both can
see (Bräuer, Call, & Tomasello, 2007; Tomasello, Call, & Hare, 2003). The implication is
that the subordinate understands that the competitor can not see the food, and strategically
targets it for retrieval. Similar results are seen in gibbons (Sánchez-Amaro, Tan, Kaufhold, &
Rossano, 2020), Tonkean macaques (Canteloup, Piraux, Poulin, & Meunier, 2016), and
even capuchins and common marmosets (Burkart & Heschl, 2007; Hare, Addessi, Call,
Tomasello, & Visalberghi, 2003). This suggests that understanding something of what others
see is at least a general anthropoid feature.
Referential pointing
Also relevant are observations of referential pointing in apes. Frans de Waal stated, “there is
no point to pointing unless one understands that the other has not seen what you have
seen” (de Waal, 2003, p. 23). Anecdotally, the majority of caged chimpanzees will point to
food visible to them outside the cage that is seemingly unnoticed by human caretakers,
clearly in an attempt to obtain the food. This behavior is untrained. There are also an-
ecdotes from the wild of chimpanzees using pointing to draw attention to other chim-
panzees (de Waal, 2003).
An experimental approach was taken by Cartmill and Byrne (2007), using orangutans.
In their study a human caretaker withheld half or all of a treat and then remained
unresponsive to food entreaties. When half the treat was withheld, the orangutans often
repeated behaviors – including pointing – that had gotten them half the treat. However,
when all of it was withheld, they tended to switch to other behaviors.
These results may indicate that the animals understood the difference between incomplete
understanding and a total lack of understanding on the part of the caretaker, prompting a
behavioral adjustment. If so, they are consistent with the existence of a theory of mind.
However, an explanation that doesn’t involve theory of mind seems equally plausible: When
something partially worked, it was repeated, but if it didn’t, it wasn’t.
Perhaps a similar repeat-if-successful explanation can account for the ability of certain
domesticated species like dogs and horses to use human cues to find food (Call et al., 2003;
Proops, Rayner, Taylor, & McComb, 2013). However, in the case of dogs, there is evidence
that young, presumably naive puppies understand pointing from the very first trial, an ability
that appears to be partially genetic (Bray et al., 2021). While that tends to disfavor a stimulus-
response explanation and favor a theory of mind (a genetic trait selected by humans?), it
remains to be seen whether similar conclusions apply to primates.
In any case, the Cartmill and Byrne study is a good illustration of the surprising difficulty
inherent in distinguishing from behavior alone, between an internal cognitive state (theory of
mind), and an internal precognitive state (e.g., stimulus-response association). This is much
the same problem, of course, that Povinelli and Bering (2003) highlighted, and that was
pointed out at the beginning of the chapter as a thorny issue when inferring conscious states
more generally.
Helping and deception

Helping behaviors and deception have also been cited as suggesting a theory of mind.
Elephants are often observed helping their disabled fellows, for example by attempts to lift a
prone body or to pull a calf from a hole (Hart, Hart, & Pinter-Wollman, 2008). Dolphins and
whales sometimes respond to distress in conspecifics by maintaining proximity or by sup-
porting the injured animal at the surface. With regard to deception, species as diverse as
hyenas and dolphins have been observed hiding objects from conspecifics (Kuczaj, Tranel,
Trone, & Hill, 2001).
Whether one accepts any of these behaviors as indicating a complex state like theory of
mind, may depend on whether the behavior is itself sufficiently complex to render a less
complex state implausible. Simple gaze following, repeating versus switching behaviors
depending on the level of success, pointing, cue use to find food, helping behaviors, and
deception may not rise to the standard required. In each case, it is not hard to imagine
instinctual or associational learning mechanisms that could produce the behavior. Many
of us may be more convinced when a chimpanzee looks around barriers to see what a
human is gazing at, or selectively targets foods that a dominant rival cannot see. In these
Consciousness 293
cases the complexity of the behavior seems to imply a more complex state we can label a
theory of mind.
However, if our main requirement is that behaviors be complex before we entertain
them as evidence, we must be prepared to accept the possibility that nonprimate species
can also have a theory of mind. Scrub-jays, for example, show surprisingly complex be-
haviors when food-caching. When observed by other jays, individuals appear to guard
against pilfering by caching food in locations (a) farther rather than closer to the observer;
(b) hidden from the observer by a barrier rather than in plain view; and (c) less illuminated
rather than more illuminated. These distinctions are not made when caching occurs in
private. Furthermore, when caching has been observed, those caches are retrieved first
when a private opportunity arises, and they are often moved to new locations (Emery,
2006). These behaviors seem sufficiently complex to indicate the existence of theory of
mind, but they may not be characteristic of the Eurasian jay, a corvid of a different genus
(Amodio, Farrar, Krupenye, Ostojić, & Clayton, 2021). Nevertheless if at least some birds
have it, then the viewpoint that it is a primate characteristic (Brüne & Brüne-Cohrs, 2006)
is obviously problematic.
Once again we seem to have little more than the encephalization hypothesis to fall back
upon in judging which species are likely to possess a consciousness-related construct. If we
accept that only complex behaviors can constitute acceptable evidence of theory of mind,
we are left with relatively complex – i.e., big-brained – animals that have it. Chimpanzees
do, given that they look around barriers to see what others are looking at, and they selectively
target food that more dominant individuals cannot see. Scrub jays do, too, given the increase
in complexity of their food-hiding behaviors when being observed. Apes and corvids, as
we have seen, are both relatively large-brained. The situation is much the same as exists in
mirror self-recognition, except that fewer species have been investigated with respect to
complex behaviors that imply theory of mind.
Conclusion
There are many conceptions of consciousness, ranging from an identification with attention,
to considering it a byproduct of large-scale systems like the totality of cognitive processes or
even of reality itself. The comparative study of consciousness introduces further uncertainties
because external behaviors are used to infer the functions of consciousness, and disagreements
often arise over the meaning of such behaviors.
Sensory awareness, while a seemingly simplistic function of consciousness, in fact is
quite informative when impaired, as in blindsight and deaf hearing. Patients who deny
seeing anything but who can localize stimuli, and others who deny hearing anything but
who orient to loud sounds, have in common a destruction of primary sensory cortex
accompanied by a lack of sensory awareness. Experiments using TMS in humans, and
disconnection of visual cortex from higher order cortex in monkeys, suggest that sensory
awareness is the result of reentrant connections from higher order cortex back to primary
cortex. These connections appear to be characteristic of mammals in general, and thus have
a 220 million year history. While it is unknown whether they supported sensory awareness
that long ago, macaques experience blindsight, putting a lower limit of about 29 million
years on the origin of sensory awareness.
In contrast, the idea that attention connotes consciousness is more problematic, in part
because it is not a unitary concept. Attention as selection, as recognition of meaning, and as
alertness are all fair characterizations, but such a subdivision greatly complicates the task of
tracing the evolution of consciousness. One of these, selection, seems especially problematic
in that it may have its origins in the first appearance of nervous systems.
Metacognition, the awareness of one’s own cognitive states and processes, includes such
phenomena as “feelings of knowing” and the ability to judge the quality of one’s retrieved
answers. Because these feelings and judgments are vague and error-prone, they can be
viewed as a kind of “fringe consciousness” constructed from unconscious processes.
Human research suggests that some forms of metacognition begin developing between 4
and 5 years of age. All great apes as well as an Old World monkey (the rhesus macaque)
show evidence of metacognition, but a New World species (the capuchin monkey) is “on
the cusp”, with studies finding either no proficiency, reduced proficiency, or proficiency
only in some individuals.
Self-recognition seems a fairly straightforward function of consciousness, in the sense that
it is easily demonstrated through self-directed responses using mirrors. It has been found in
apes, Asian elephants, and horses, and perhaps in siamangs, dolphins, corvids, and cleaner
wrasses. Apes, which have been most extensively tested, show individual differences in that
about a quarter of adolescents and young adults, and three-quarters of older adults, fail to self-
recognize. This effect appears to be at least partially developmental in that some animals that
self-recognize earlier in life fail to do so later. Many individuals never succeed in recognizing
themselves. These observations suggest that apes may be barely over an evolutionary divide
that excludes some individuals as well as Old and New World monkeys.
Encephalization may well play a role, in that most (but not all) self-recognizing species
have relatively high encephalization quotients. Research on chimpanzees suggests that there
may also be important roles for brain connectivity, specifically between the parietal and
frontal lobes; and sociality, with self-recognizing individuals showing greater social ability.
Theory of mind is often taken as a manifestation of self-awareness, on the grounds that
imputing a state of knowledge in others presupposes understanding similar states in oneself.
Some simple behaviors that might be taken as implying a theory of mind, such as gaze
following, helping behaviors, and deception, are widespread among animal species, but are
also potentially interpretable in stimulus-response or instinctual terms. More complex
behaviors, such as approaching and looking around a barrier to see what a human is staring
at, or selectively targeting foods that a dominant rival cannot see, seem more convincing of
a theory of mind. Certainly a number of primate species perform one or both of these,
suggesting that theory of mind is a general anthropoid feature. However, scrub jays also
engage in surprisingly complex alterations of behavior when food-caching, depending on
whether or not they are being observed by other jays. This again suggests a possible link to
encephalization.
Thus, in the end, evolutionary analyses appear to confirm the multifaceted nature of
consciousness. Selective attention may be as ancient as nervous systems, and sensory
awareness possibly traces to the first mammals. But, in any case, sensory awareness certainly
originated earlier than self-recognition.
17 A summary in nine firsts
The roots of cognition date nearly from the origin of life a little over four billion years ago.
When the first cell responded to interior pressure and expelled waste products, a primitive
type of sensation was born. Emerging about the same time was the ability to pass useful
substances into the cell while excluding less useful ones. Soon, the addition of flagella or cilia
allowed movement away from less- to more-productive areas. Together, internal mechanical
sensing, external chemical sensing, and the ability to move constituted the first building
blocks of cognition.
Over 600 million years ago, hair-based mechanoreceptors were incorporated into the
stinging cells of jellyfish and other cnidarians. Neurons may have evolved from them, with
neural nets emerging by 605 million years ago. A little later, early chordates had sensing hair
cells and a nervous system. The nervous system in turn enabled the selection of one of
multiple stimuli, an early form of selective attention. Early nervous systems, however, de-
pended on primary sensory cells with sensors and an axon on opposite ends, limiting their
architectural complexity.
Metazoan vision likely appeared first in cnidarians. Whether vertebrate eyes descended
directly from them is unclear, but all eyes use variations of vitamin A-based photopigment.
An additional photopigment class, the flavins, originated even before cnidarians and was later
used to regulate circadian rhythms.
Paired, pigmented though likely lensless cup eyes probably emerged with the first bi-
lateria by about 580 million years ago. Early chordates likely had only one eye, used for
sensing direction. Optical reversal in the eye resulted in a nervous system crossover, with
the left side of the world represented on the right side of the nervous system, and vice
versa. It seems likely that this scheme was simply duplicated when eyes again paired in
vertebrates.
One “backward” aspect of the visual system, namely the slowing rather than initiation of
neurotransmitter flow in response to light, was probably in place in chordates. Multiple cone
types likely date to the vertebrate emergence.
The ability to move is thought to have been characteristic of early metazoa as early as
650–780 million years ago, specifically in swimming sponge larvae. It was accomplished with
beating cilia, propelling free-swimming forms through water, or a little later, in benthic
species, over a mucus-lubricated trail. Ancestral flatworms both crept on the sea bottom and
used muscles for full-body undulation when swimming, prior to 540 million years ago.
The ability to remember was probably present even in early single-cell organisms, in the
form of habituation to repeated stimuli. Conditioning dates at least from the cnidarian
emergence over 605 million years ago. It was the product of a central nervous system or-
ganized to allow the arbitrary pairing of stimuli and responses. Visual sensory memory,
produced as an aftereffect of neural activity, likely originated with the first cnidarian eyes and
in all probability was present in chordates.
DOI: 10.4324/9781003137863-20
These characteristics – receptors linking to nervous systems enabling sensory selectivity;
the ability to move through water either in suspension or on the ocean bottom; and the
beginnings of sensory memory – were the birthright of chordates. From those beginnings
sprang numerous cognitive mechanisms and cognitive-influenced behaviors. These may be
loosely organized under nine “firsts”.
The first vertebrate (520 million years ago)

The first vertebrate was a jawless fish with a cartilage-like notochord extending to the head,
which housed a brain. Close descendants had hard teeth formed of dentine. A nervous system
was present that included the beginnings of the cerebral hemispheres. Sensory cells with
sensory and synaptic ends allowed a more complicated neural architecture than previously
possible.
Sensory capabilities included a vestibular sense based on one semicircular canal within an
inner ear. A second canal would soon form in most vertebrate descendants. There were
probably olfactory nerves, an olfactory bulb, and external nostrils. Bitter taste receptor genes
had evolved, and taste buds would soon emerge. Vision probably used paired, optically
reversing, moveable eyes. Each eye had a retina with both rods and multiple cone types, and
a macula for more acute vision.
Crossover existed in a portion of the motor system, and as that strengthened it brought
each side of the world into visual and motoric alignment in the opposite cerebral hemisphere.
Meanwhile partial crossover coordinated movement between the body’s sides. An evolving
cerebellum in most descendants, initially composed of only a few cells, soon contributed to
consistent mapping of the sensory and motoric worlds.
Following upon conditioning, long established as a form of memory, discrimination
learning allowed beneficial and noxious stimuli to be distinguished and responded to
appropriately.
The first tetrapod (365 million years ago)

The first tetrapod was an amphibian resembling the closely related lungfish. In place of the
lungfish’s fleshy, lobed body fins were crude limbs and digits that propped the head up in
shallow water, allowing air breathing.
Three semicircular canals in the inner ear provided a fine sense of balance. Also present was a
basilar membrane embedded with basilar papillae, for transducing sound. However, the middle
ear contained only one ossicle, limiting the high frequencies that could be heard. Olfactory
genes allowed a range of odors to be detected, and would soon vastly expand in number.
Several changes occurred during the transition from direct tail-based propulsion in water
to the use of limbs on land. “Rear-wheel drive” evolved from earlier “front-wheel drive”,
with the tail used to anchor muscles connected to the rear limbs. Muscles and bones enlarged
to provide body support, and the limbs shifted laterally, allowing a sprawling gait with
symmetric alternation of sides.
A hippocampus was present, having expanded from the few cells in bony fish ancestors.
Although its functional significance at that time is unclear, one function of the present-day
hippocampus is to support episodic memory.
The first eutherian (170 million years ago)

The first eutherian weighed less than an ounce, but had a relatively large brain for its size.
Its middle ear ossicles had separated from the jaw bone, and it probably had fur, both
A summary in nine firsts 297
characteristics identifying it as a mammal. Its nocturnal existence was a factor in encouraging
the evolution of intelligence as well as sharp senses of hearing, touch, and smell.
With respect to hearing, all three ossicles were in place, allowing the impedance of air
to be matched to that of fluid in the inner ear. A fully coiled basilar membrane also existed.
As a result, sound could be heard with considerable sensitivity, with an upper-extended
frequency response and with improved sound localization.
Tactile sense developments included Meissner’s corpuscles in the skin to detect texture and
primary and secondary somatosensory cortex in the parietal cortex.
The olfactory bulbs had undergone multiple expansions. Bitter taste pseudogene for-
mation had increased relative to earlier tetrapods, perhaps due to a decreased dietary
reliance on plants.
Visually, two of four cone types had been lost as unnecessary metabolic expenses, in that
early nocturnal mammals relied more on rod-based night vision than on cone-based day
vision. In the brain, areas V1 and V2 had formed, respectively reflecting increased processing
of visual features and contours, and of figure-ground segregation. The aftereffects of neural
activity in V1 provided a brain-based component of visual sensory memory.
Area VP/V3 had evolved for increased processing of visual form. Reentrant connections
between forward areas of the brain and V1 may have supported sensory awareness.
Movement involved a largely but not fully erect body posture, with weight distributed
more directly over the legs. An asymmetrical gait, with different timing cycles for the
front and rear limbs, likely supplemented symmetrical ones, resulting in higher speeds.
These and other movements no doubt benefitted from the recently evolved primary
motor cortex.
The first primate (74 million years ago)

Although primates left no fossils until about eight million years after their origin, the earliest
ones may have resembled small squirrels in size and body plan. They had mobile, grasping
hands and feet, with relatively flat nails on some digits, and opposable thumbs and big toes.
A reduction of the olfactory bulbs would soon begin in most of the order, indicating less
reliance on smell and an increasing dependence on vision. Early primates probably had large
corneas for improved light-gathering, reflecting their nocturnal lifestyle. They had evolved,
or would soon evolve, a tapetum lucidum to further increase light sensitivity. A fovea
supporting high-resolution vision would soon develop, although it would be ill-defined and
partially occluded by blood vessels. There was substantial binocular convergence, providing
good depth perception for insect predation.
Movement adaptations included, or would soon include, mobile ankles allowing the
grasping of vertical supports as well as leaping. Within a few million years, among anthropoid
descendants, this would transition to walking. It involved an ambling, diagonal gait with
extended strides, appropriate to a fine-branch environment, aided by a large, heavy tail that
helped maintain balance on branches.
In the brain, supplementary, premotor, and parietal motor areas had evolved and become
interconnected for greater movement control. There may also have been a weak population
left-handedness in manual actions.
The equivalent of human area MT/V5 had evolved to support motion perception. Early
primates likely also had the ability to follow gaze. Patches of cortex recognized classes of
objects, including face patches that were configuration-based and orientation-specific. If
episodic memory had not already evolved with tetrapods, it probably existed in early pri-
mates. By this time, the hippocampus also possessed place cells and grid cells, which were
used to represent the spatial environment.
The first ape (29 million years ago)
The first ape undoubtedly resembled Aegyptopithecus, the possible monkey-ape common
ancestor. If so, it weighed about 6 kg (13 pounds) and had a brain 30 cubic centimeters in
size, resulting in an EQ of a little under 3 when calculated using a primate-appropriate
exponent. It had the heavy limbs of a slowly moving arboreal quadruped. It had a tail, but
that would soon be lost by its descendants, possibly because it served no useful function in
countering the movements of a heavier body.
The olfactory bulbs had further decreased in size, accompanied by increased olfactory gene
deactivation, and the vomeronasal nerves had been lost. These circumstances point to a
reduced reliance on odors.
The visual system showed substantial change. A third cone type had re-evolved for better
color vision. The tapetum lucidum had been lost, and the cornea and lens had reduced in
size, so that the eye had less light-gathering power but produced a sharper image. The
unoccluded fovea was well-defined, and there was an enlarged optic nerve. All of this is
consistent with a visually dependent, diurnal, probably frugivorous lifestyle.
In the brain, the visual areas had enlarged, and depth was perceived with considerable
accuracy aided by increased binocular convergence. The ventral parietal cortex was in place
and was sensitive to visual flow.
Visual selectivity had increased due to a narrowing of the field of best vision.
Accompanying it, sound could be localized with high accuracy. Improved cross-modal in-
tegration of sensory information was served by the brain’s intraparietal sulcus, which also
processed egocentric location. Concomitantly it was involved in controlling eye movements
and in deploying attention.
The inferior parietal lobe was involved in visual enumeration, and a subitizing process
based on analog quantities was in place to quickly enumerate small numbers of stimuli.
Mental maps were used in navigation, supported by the parietal lobe. The left inferior parietal
lobe had especially enlarged and was probably used both in spatial attention and in reaching
and grasping.
Ventral visual pathways had also further developed. The first ape may have had an area V4
capable of perceiving curvatures in depth and color, and an IT/LOC area that recognized
both two- and three-dimensional patterns with movement. Perceptual invariance was in
place. However, there was probably little if any global-over-local bias. Recognition did not
exist of mirror images of the self in reflecting pools of water, even though something
“different” may have been perceived about them.
Motor planning and movement complexity had increased, aided by premotor cortex that
controlled both proximal and distal muscles, and by an enlarged cerebellum. Population
right-handedness had likely emerged in unskilled reaching, gesturing, and feeding behaviors.
This was possibly accompanied by a leftward asymmetry in the hand area of the primary
motor cortex. However, population left-handedness probably existed for extractive actions
similar to that of the tube task.
Several brain areas had evolved that would figure into the acquisition of language.
Broca’s area existed in the form of homologs to areas 44 and 45, and area 6 regulated
laryngeal vocalization. A larger left- than right-sided planum temporale was in place.
There was also a right ear advantage over the left in recognizing vocalizations, although
that may have owed less to the planum temporale that it did to the anterior superior
temporal gyrus.
A short-term memory lasting a number of seconds existed, in part supported by areas 9 and
46 in the brain. A “local” type of semantic memory was also present, involving perirhinal
cortex. It represented particular classes of objects, but was not yet modality-free.
Although the first ape showed no inkling of self recognition, it nevertheless exhibited
metacognition by knowing to withhold a response when it judged its knowledge to be
insufficient.
The first great ape (20 million years ago)

The first great ape likely resembled Proconsul and Morotopithecus, with a greatly increased
body weight somewhere between 15 and 45 kg (30–100 pounds). Its brain was probably
170–370 cubic centimeters in size, resulting in an EQ in the range of 11 to 18. It was arboreal
and frugivorous, although whether it primarily locomoted above- or below-branch is un-
clear. Either way, it could probably adopt eccentric grasping postures, allowing suspension
from multiple limb supports and thus access to fruit at the periphery of trees. Sensory
capabilities had not changed much since the first ape.
Population left-handedness in tube-type extraction tasks had likely evolved, but in a
few million years, would switch weakly to the right in most of the first great ape’s
descendants. This upcoming change, largely involving the left hemisphere of the brain,
probably co-occurred with the ability to use a simple set of communication gestures
similar to the naturally occurring gestures of living great apes. A rudimentary grammar
may have evolved at the same time, perhaps initially limited to ordering a very small
number of relatively meaningless phonological elements, but coming to be applied in an
equally limited way to gestures.
Simple tools were likely created from vegetation, using an ability to form secondary
representations of not-yet-existing, hypothetical objects. Planning existed in the form of
simple scripts, enabled by the brain’s enlarged area 10. Causal relationships were
beginning to be understood, but only in a very limited way. The beginnings of a self-
concept may also have existed in the form of self-recognition of mirror images by some
individuals.
The first hominin (7.5 million years ago)

The first hominin weighed perhaps 45 kg (100 pounds) and had a roughly 370 cubic cen-
timeter brain, with an EQ of about 18. It probably locomoted using a combination of above-
and below-branch arboreality and (most significantly) bipedalism. Bipedal walking was likely
hampered to some extent by a modestly splayed, sometimes dragging hallux, and was ac-
companied by side-to-side rocking. The trunk, however, was vertical while walking, or soon
would be in the line leading to modern humans.
The arms, freed by bipedalism, could carry limited loads. Those included simple tools
made from vegetation, such as sticks for food extraction and hunting weapons like spears or
clubs. Natural stones could also be carried, to be used as hammers and anvils. In fact different
groups of the first hominins likely had tool cultures that were transmitted within and
between groups.
Objects were held in a strong, precision finger-to-thumb grip, possibly pad-to-pad, and to
some extent, preferentially by the right hand. Tube-type tasks had become predominantly
right-handed, although a complex insertion-turning component of handedness remained
mostly left-handed. A second increase in area 10 size and connectivity may have occurred,
improving planning.
Visually, a weak global-over-local bias existed, that would subsequently strengthen. The
first hominin could likely understand spatial representations to some extent, and the enu-
merating subitizing process had expanded to three to four items. Face patches in the brain
showed increased orientation specificity, responding mostly to upright faces.
A rudimentary ability to understand symbolic hierarchies existed, such as that involved in
wedge-anvil-nut-hammer constructions. This ability assisted communication using vocali-
zations and gestures, the latter having become primarily manual following the mixed manual
and nonmanual (body and head) gestures used by the last chimpanzee-human common
ancestor. Vocalizations and gestures were partially controlled by an area F5/44 that was likely
larger on the left side of the brain. Broca’s cap may have started to appear in some cases.
Finally, the proportion of individuals able to self-recognize had increased, suggesting in-
creased self-awareness. Concomitantly, it was possible to have a rudimentary theory of the
mind of others, as indicated by looking around barriers to see what others could see, or by
strategically targeting what food competitors could not see.
The first human (2.4 million years ago)

The first human, i.e., the first member of the genus Homo, weighed about 35 kg (80 pounds)
and had a 610-cubic-centimeter brain, yielding an EQ somewhat above 30. It had a stiffer
and less compliant bipedal gait than its ancestors, recovering more energy between steps. It
had an arched foot, as well as the beginning of endurance running adaptations such as
shortened toes. The pelvis had become more cup-like, cradling the internal organs. It also
provided attachments for expanded butt muscles, enabling a stable, nonrocking stride. The
fingers were straighter, accompanying reduced arboreal abilities.
Reshaping of the thumb was well underway, with the metacarpal bone developing a flatter
head and producing a firmer grasp. Perhaps as a result, worked stone tools had existed for
some time and would soon show increasing symmetry. All components of handedness
showed or would soon show a strong population trend to the right. Toolmaking involved
greater planning, aided by new inferior parietal gyri that allowed improvements in copying
gestures and understanding physical causality. Butchery was practiced, and wood was either
being chopped or soon would be. However, the use of fire lay a million years in the future.
Broca’s cap was more consistently in evidence, although the size of Broca’s area was not
yet fixed and depended on brain size. Many other language-related changes had not yet
occurred, so if language was produced, any vocal component had probably not advanced
much beyond that possessed by the first hominin. Communication gestures may have done
so, though, given the aforementioned inferior parietal lobe developments.
The first modern human (200,000 years ago)

The first modern human weighed about 55 kg (120 pounds) and had a brain around 1350
cubic centimeters, for an EQ of about 64. It had a stiff, noncompliant gait with a minimally
splayed hallux, and a cylindrical rather than cone-shaped ribcage that aided endurance
running. Most body hair had long been lost, and the first modern human’s descendants
would soon adopt clothing.
Tools were increasingly sophisticated, and included symmetrical handaxes as well as spears
with hafted points for hunting. Tool use was aided by an increased overlap of motion and
form processing in the brain.
There had been substantial olfactory pseudogene formation, continuing the trend toward
increased reliance on vision. Reflecting that, the field of best vision had narrowed to 1.5°,
and auditory localization abilities had followed suit to match.
Nevertheless, the occipital lobe had decreased in size relative to the rest of the brain,
accompanied by an extreme expansion of the parietal lobe. There was a strong global-
over-local bias in visual processing, and face patches had become widespread and more
differentiated.
Numerous adaptations were in place to serve language. Area 4 in the frontal lobe had
exerted predominant control of the larynx, and was strongly connected to parietal cortex as
well as to the nucleus ambiguous for fast control of vocalizations. The size of Broca’s area
had long stabilized irrespective of brain size. The FOXP2 gene had mutated since the last
common ancestor of chimpanzees and humans, affecting the language-related expression of
Broca’s area. There were massive arcuate fasciculus connections between Broca’s area and the
middle and inferior temporal gyri, supporting lexical-semantic processing. Accompanying
this was probably a greatly expanded vocabulary. Wernicke’s area was likely being used
in language.
Cranial, throat, and chest anatomy had evolved to support language as well. The face had
flattened and the jaw and tongue had shortened, allowing more distinctive speech sounds.
The “inverted T” of the chin had evolved, reducing stress on the chin during speech. The
vocal cavities had become relatively more vertical, supporting a deeper tongue root and
increasing the intelligibility of vowel sounds. At some point, the “bubble” on the hyoid bone
had also been lost, likewise allowing more distinctive speech. The thoracic nerves had en-
larged for breathing control during vocalization. Finally, the structure of the ear had changed
to better accommodate the perception of modern speech sounds.
Memory had improved in at least two ways. Short-term memory duration had increased
relative to that in monkeys, possibly due to participation of brain areas 10, 44, and 6. A
modality-free, general semantic memory had also emerged, using lateral temporal cortex that
was strongly connected to frontal language areas.
The continuing story

Change, of course, did not end with the first modern human. Indeed, except for limited tool
cultures, virtually all cultural developments lay in the future. To name just a few, they
included the development of all existing languages, the emergence and elaboration of dec-
orative artifacts, the shift from hunting to agriculture, the invention of philosophy, religion,
and the sciences, as well as all of the technological artifacts that both enrich and clutter our
lives. To take one modest example, it took virtually all of the remaining 200,000 years to
develop papermaking and crayons, so that a six-year-old girl could draw a picture of a
monkey and banana using the secondary representation capabilities that had begun evolving
by the lifetime of the first great ape.
How much of this explosion in culture was evolutionary? It is, of course, very hard to say.
Nevertheless, it is difficult to believe that we passed from Acheulean handaxes to Swiss Army
knives without at least some genetically based neurological change. Unfortunately, what we
can derive from endocasts is insufficient to address the question. Nor are comparative
methods available, because our hominin ancestors did not spin off any living descendants that
are genetically isolated from us.
Yet, it is important to keep in mind that whatever else we are, we are the product of
environment. If natural selection means anything, it means that if our species survives but our
environment changes, selection pressures should cause us to change as an inevitable genetic
consequence. The environment has already changed radically with the shift to sedentary
occupations and lifestyles, the increasing substitution of corporate agriculture for family
farming, and the development of small communities and then larger cities that service every
need through occupational specialization.
One physical result is that our bones have weakened. The bending strength of the femur
and tibia declined as much as 20–30% between the Upper Paleolithic and the Iron age/
Roman periods, i.e., between roughly 22,000 and 2,000 years ago. Ruff et al. (2015) at-
tributed it to a shift from a more mobile to a more sedentary lifestyle as agriculture began.
They viewed this as more environmental than genetic, with sedentary lifestyles resulting in a
load reduction that limited bone development during the lifespan. However, there is nothing
to preclude a possible shift in gene frequencies accompanying the weakening, lending it a
partially genetic character. After all, one would expect that any genetic coding for stronger
bones would be selected against if they were no longer required (cf. Chirchir et al., 2015,
who acknowledged a similar point). Further weakening down to modern times may have
continued as a trend, although it has been too small to reach the threshold of statistical
significance (Ruff et al., 2015).
The problem is that identifying shifting traits alone does not separate environmental from
genetic influences. It may be more useful to examine how traits are affected by changing
gene frequencies. An example in northern Europe is the frequency of a gene, designated
−13,910∗T, for lactase persistence, i.e., for an enzyme allowing adults to digest the sugar
(lactose) present in milk. The emergence of the gene accompanied the shift from a hunter-
and-gatherer lifestyle prior to 8,400 years ago to a predominantly sedentary, farming lifestyle
4,000–6,000 years ago (Gerbault et al., 2011). Molecular evidence suggests that the gene first
appeared about 6,000 years ago, roughly when milk began to be collected (Segurel et al.,
2020). Presently, only a few thousand years later, over 90% of northern Europeans carry the
gene, indicating its frequency must have dramatically increased across time and space under
strong selective pressure. Yet even today, 65% of the world’s people have no lactase persis-
tence. That is likely to continue to change as −13,190∗T and other persistence genes spread
and are selected for (Gerbault et al., 2011).
Gene frequency studies also indicate strong recent selection for reduced pigmentation in
western Eurasia. Wilde and colleagues extracted DNA from 63 individuals dating from 4,000
to 6,500 years ago, mostly from modern-day Ukraine, and compared it to modern Ukrainian
as well as more general European populations (Wilde et al., 2014). Alleles associated with
lighter skin, hair, and eyes were found to have increased in frequency, with high selection
pressure. The effects have been dramatic, showing increases from 4% to 37%, 16% to 71%,
and 43% to 97% in the percentage of individuals with three light-pigmentation alleles, be-
tween the ancient sample and modern Europeans (with slightly smaller increases compared to
modern Ukrainians). Among the reasons proposed by the authors for the shift toward lighter
coloration was that it was an adaptation to reduced sunlight at high latitudes. Light-colored
skin increased the absorption of sunlight, maintaining vitamin D synthesis under low-light
conditions.
Recently, Field and colleagues developed a powerful new technique for detecting rela-
tively recent mutations. It exploits the fact that locations on chromosomes near a recent
mutation are relatively unlikely to have sustained recent mutations themselves; conversely,
locations near an older mutation are much more likely to have sustained them due to the
passage of time. Therefore, as a first approximation, determining the distance between
mutations on either side of a third one, indexes the amount of time since the third mutation,
with longer distances indicating that it occurred correspondingly recently. Finally, the fre-
quency of the third mutation in the population is determined, and that along with the time
determination allows an estimate of selection pressure (Field et al., 2016).
Using this strategy, Field et al. confirmed that lactase persistence and light pigmentation
have been under heavy positive selective pressure. Also under positive pressure are height,
infant head circumference, decreased body mass index in males, female hip size, and later
sexual maturation in females.
However, it is not clear whether all human populations are showing the same trends
(Field et al., 2016). This raises an important point: The mere fact of genetic change does not
necessarily mean that the species as a whole is changing. It remains to be seen, for example,
whether lactase persistence becomes a universal human trait. Lighter pigmentation almost
certainly will not, because people at more tropical latitudes derive benefits from heavier
pigmentation, such as a limit on the harmful effects of solar radiation (Jablonski &
Chaplin, 2017). In fact, this is clear in the data of Wilde et al. (2014), in which all three
low-pigmentation alleles were found to have near-zero frequencies in Asian and African
populations.
A better candidate for a future species-wide characteristic, and importantly, one with
cognitive implications, might be a bigger head at birth. A larger infant head circumference
was one of the characteristics identified by Field et al. (2016) as being under strong selective
pressure. Presumably, this is universally beneficial due to a larger brain. But to be fully
realized, will universal Caesarian birth be required to escape pelvic size limits? That would
require the easy availability of the surgical procedure on a worldwide scale, regardless of
individual economic circumstances. If that problem is overcome, then over the long run, the
brain of our species will be free to evolve greater cognitive complexity.
Our inability to envision whether that is even feasible points to the heart of the problem of
predicting evolution. For our capacity to do so, even in general outline, is limited by the
feebleness of our insight into the future. All we can be sure of is that as the environment
changes, so must we.
Glossary
Acheulean a hominid tool culture that began about 1.8 million years ago, marked by the
rise of handaxes
acritarchs tiny acid-resistant fossils showing evidence of a cell wall
acuity the ability to resolve fine visual details
adductors in the leg, muscles on the inside of the thigh that move it inward
agonist a drug that temporarily binds to neural receptors and prevents their normal
function
agrammatism a clinical disorder marked by the disordering of syntax (or grammar)
Ahrensburgian a human tool culture known for extensive organic remains, and for
showing evidence of hunting using spear-throwers or bows and arrows
allele a variation of a gene
allocentric frame of reference a mental framework allowing judgment of location
relative to the environment
allopatric speciation the evolution of new species by physical separation
amino acids the building blocks of proteins
amniotes animals whose embryos develop within a membrane
anaerobic living without oxygen
anapsids tetrapods with no openings in the side of the skull behind the eyes
anterior forward
Anthropoidea anthropoids, i.e., monkeys, apes, and man
arboreal living in trees
archaea a domain and kingdom of single-cell organism
artifactual pertaining to an artifact, such as a stone tool
artiodactyls a clade within mammals, consisting of mammals that are hooved and have an
even number of toes
association the arbitrary pairing of a stimulus with a response in memory
asymmetrical gait a gait with a movement cycle taking a different length of time for the
forelimbs and hindlimbs
atrophy shrinkage
auditory sense the sense of hearing
Aurignacian a human tool culture marked by an increase in microblades and microliths
autosomal pertaining to the autosomes
autosomes all of the chromosomes other than X and Y
axon a long thread-like projection of a neuron
backed blade a stone blade blunted on one edge
basilar membrane a membrane with hair cells, located inside the cochlea
basilar papillae rounded projections in the inner ear, each containing a few hair cells
benthic bottom-dwelling
Glossary 305
bilateral two-sided
Bilateria bilaterally symmetric animals
bilayers films
binocular convergence the state of both eyes imaging the same object at the same time
binocular cue a depth cue requiring two eyes to see
binocular disparity a binocular depth cue using the discrepancy between images from
the two eyes
binocular field of view (BFOV) the opening angle of the joint field of view of the two
eyes
biofilms cooperative communities of bacteria
biomineralization the incorporation of minerals into structures such as bones or teeth
bipedal two-legged; walking on two legs
bipolar cells a class of neurons located in front of the retina that connect the ganglion cells
to the rods and cones
blindsight a phenomenon in which an observer claims to be blind, yet shows residual
visual abilities
brachiation a form of locomotion characterized by swinging from branch to branch
Broca’s cap an outward bulge of cortex in Broca’s area
Cacatuidae the family of cockatoos
Cambrian explosion the rapid expansion of metazoan phyla in a portion of the Cambrian
period, roughly 520 or 530 to 540 million years ago
catalyze accelerate, especially a chemical reaction
Catarrhini narrow-nosed monkeys; also known as Old World monkeys
caudal rear
caudofemoralis longus in most tailed animals, a muscle located largely in the tail and
connected to bones of the rear limb
Cercopithecidae a family of catarrhines consisting of two subfamilies, the
Cercopithecinae and the Colobinae
Cercopithecinae a subfamily of Cercopithecidae consisting of macaques, baboons, and
vervet monkeys
Chordata, or chordates relatively complex animals with a hollow neural tube behind a
notochord
cilia small hairlike cellular outgrowths
circadian rhythm a biological rhythm governing our sensitivity to the 24-hour day
clade a branch on the tree of life defined by a novel charateristic
cladistics the grouping of species by novel characteristics not present in other less-related
species
Clovis a North American tool culture involving hunting large game
cnidarians a phylum of animals composed of jellyfish, hydras, sea anemones, etc.
coalescence time the last date at which two later species had completely common an-
cestry
cochlea a spiral-shaped cavity of the inner ear
Colobinae a diverse subfamily of Cercopithecidae that includes colobus and proboscis
monkeys, doucs, langurs, etc.
complex cells in the visual system, neurons that respond to orientation over a large area,
and often to movement in a particular direction
composite tools tools made of more than one material
concordant using the same side, as in two right-handed siblings
cones a class of receptors in the retina, chiefly responsible for color vision
conspecifics other members of the same species
306 Glossary
contralateral opposite-sided
convergent evolution the evolution of similar form or behavior in relatively unrelated
species, due to similar environmental pressures
core in the making of stone tools, the stone from which the tool is made
coronal organ a vibration-sensing organ in some chordates, located in the oral region
cortical magnification factor a mathematical relationship between the acuteness of an
area of vision and the amount of cortex that processes it
corticospinal tract a motor tract originating in the precentral gyrus of the brain that
crosses over to the opposite side of the body; also known as the pyramidal or dorsolateral
tract
Corvidae the family of corvids, which includes crows, ravens, and jays among others
cranial nerves sensory and motor nerves completely located in the head
craniates animals with skulls
cranium bony braincase
crown group one of at least two subgroups with living descendants
cryptochromes a class of photopigments, more recently called flavins
ctenophores comb jellies
cubozoans box jellyfish
cultural variation in ape communities, the extent to which a behavior differs between
communities
cutaneous nerves nerves serving somatosensation, which enter the spinal cord
deaf hearing a phenomenon in which the patient denies hearing anything, but never-
theless orients to loud sounds
dendritic arbor the treelike branching of dendrites
dental comb outward-projecting lower canines and incisors, used as a comb while
grooming
dentine bonelike tissue without cells
dentition the form and patterning of teeth
derived character a characteristic possessed by one subgroup but not all subgroups within
a clade
descent with modification the intergenerational transfer of genetic instructions that
differ between parents and offspring
diapsids tetrapods with two openings in the skull behind the eye
dichromacy the state of having two types of cones
diffusion in ape communities, the social transmission of behaviors across communities
dinoflagellates ocean-dwelling unicellular organisms with two flagella
distal farther from the core
diurnal active in daytime
dizygotic twins nonidentical (fraternal) twins
dorsal top
dorsal visual stream the visual pathway from brain area V1 to the parietal lobe
dorsolateral tract a motor tract originating in the precentral gyrus of the brain, that
crosses over to the opposite side of the body; also known as the corticospinal or pyr-
amidal tract
echo the auditory form of sensory memory
ectoderm in vertebrate prenatal development, the cells giving rise to external features like
the skin, nails, and hair, as well as the brain and nervous system
egocentric frame of reference a mental framework allowing judgment of location re-
lative to the body
Glossary 307
elaborative rehearsal processing the meaning of items to be remembered, thus associating
them to the existing knowledge structure
encephalization quotient (EQ) a calculated quantity expressing brain size in a form that
takes the brain-body size relationship into account
endocast a latex rubber molding of the inside of a skull; or more recently, a virtual
rendition of the inside of a skull using imaging data
endothermy a state characterized by the internal generation of heat to maintain body
temperature, i.e., “warm-bloodedness”
episodic memory memory for episodes or particular events in the past
eukaryotes literally, “true kernels”, i.e., cells having nuclei
eumetazoa all animals that are not sponges
eutheria literally, “true beasts”, i.e., placental mammals
exome the reduced portion of the genome that codes for proteins
extralemniscal system somatosensory neural pathways that run upward to secondary
somatosensory cortex
extrapyramidal tract a collective term for motor pathways with only partial crossover
between the brain and the body
factor analysis a statistical technique that groups tasks or measures according to their
interrelationships
fatty acids a class of lipids
femur the thigh bone that forms a ball joint with a socket in the pelvis
figure-ground segregation in vision, the process of extracting an object from its back-
ground
flagella whip-like cell structures
flakes in the making of stone tools, the stone fragments struck from the core
flavins a class of photopigments
flexed bent
focal length the distance required for an image to come to a focus
folivores leaf eaters
foramen magnum the opening on the bottom of the skull allowing entry of the spinal
column
fovea the central area of maximally acute vision located within the macula
frontal eye field a location in the frontal lobe of the brain involved in making voluntary
saccades
frontal pole the foremost part of the frontal lobe
frugivorous eating fruit
functional magnetic resonance imaging (fMRI) a method for imaging brain activity
involving detection of electrical currents influenced by proton spin
gait the cyclical means by which the limbs move the body
ganglia functional groupings of nerve cells
ganglion cells a class of neurons located in front of the retina, whose axons form the optic
nerve
gating the controlled passing of substances through a membrane
generator potential a net positive electrical charge inside a neuron, that has increased past
a threshold value, opening sodium channels in the cell membrane
genetic recombination an error during the reproduction of chromosomes resulting in
the movement of genetic instructions from one chromosome to another
geniculostriate route a visual pathway that proceeds from the eye to the lateral geniculate
nucleus to the primary visual cortex
genome the set of genetic instructions; all the chromosomes together
308 Glossary
gill arches thin support structures for the gills, made of cartilage or bone
global precedence effect in its first sense, faster response to global (broad) than to local
(narrow) aspects of a scene; in its second sense, the greater effect of conflicting in-
formation at the global level on the local level, than vice versa
gluteus maximus muscles large muscles in the butt that allow us to walk stably
gnostic cell, or grandmother cell in vision, a neuron that responds to a specific object,
such as one’s grandmother
gracile slender
grammar, or syntax the rule-based organization of symbols in orders that succeed in
conveying meaning
grandmother cell, or gnostic cell in vision, a neuron that responds to a specific object,
such as one’s grandmother
Gravettian (called Périgordian in France) a human tool culture characterized by
backed blades and end-scrapers
grid cells neurons that respond to locations in an overall grid representation of the en-
vironment
gustatory sense, or gustation the sense of taste
habituation a decline in response to repeated stimulation
hair follicle receptors nerve endings wrapped around the base of a hair, that respond to
its bending
hallux big toe
Hamburgian a human tool culture known for extensive organic remains, and for showing
evidence of hunting using spear-throwers or bows and arrows
hamstrings muscles on the back of the thigh that move it backward
Haplorhini, or haplorhines dry-nosed primates
heading the direction of movement; bearing
height in the visual field a monocular depth cue in which the images of objects lower in
the visual field are usually judged closer than those higher in the visual field
Heschl’s gyrus a gyrus on the superior surface of the temporal lobe that constitutes the
primary auditory area
heuristics rules of thumb that tend toward the solution of a problem
Homeobox genes genes “like a box”, because the DNA sequence is short and can be
enclosed by a box in written form
hominid in outmoded usage, humans and their immediate ancestors; now used synony-
mously with Hominidae
Hominidae a family consisting of all great apes including humans
Homininae a subfamily consisting of all African apes including humans
Hominini, or hominins a tribe consisting of all bipedal apes including humans
Hominoidea, or hominoids the superfamily consisting of apes including humans
homologous traceable from common origins
homology a similarity in traits traceable to common ancestry
horizontal gene transfer the movement of genetic material from one organism to an-
other in the absence of a parent–child relationship
Hox abbreviation of Homeobox
humerus the upper arm bone
hyoid a horseshoe-shaped bone in the neck
hypercomplex cells in the visual system, neurons that respond to edges having both an
orientation and an end; some also respond to curvature
hyperpolarize to become more negatively charged
icon the visual form of sensory memory
Glossary 309
ilium each of the bladelike extensions at the back of the pelvis
impedance the amount of pressure required to produce a given displacement
incus literally, “anvil”; one of the ossicles of the middle ear
insectivores insect eaters
interneurons small, laterally connecting neurons
interorbital distance the space between the eyes, measured between their nearest edges
ions electrically charged atoms
ipsilateral same-sided
ischial callosities callused skin patches on the buttocks that serve as padding while sitting
island dwarfism the state of having reduced size, due to the species’ isolation on an island
over time
kinesthetic sense a mechanical sense that assesses joint position and muscle tension
knapping the act of shaping a stone core by breaking off flakes
lactase persistence the presence of lactase beyond childhood and into adulthood, al-
lowing the digestion of the sugar lactose, present in milk
laryngeal motor cortex cortex involved in regulating the larynx
lateral line system in fish, hair cells arranged in a line from gills to tail, detecting pressure
gradients
lateral pallium a brain structure in fish that is anatomically, genetically, and functionally
homologous to the avian and mammalian hippocampus
lesions areas of physical damage, in the brain usually resulting from strokes or penetrating
wounds
Levallois technique a stone toolmaking technique involving removing many flakes from
a core in preparation for striking off one desired flake
lexigram a type of visual symbol conveying meaning
lipids fatty or waxy molecules
locomotion movement from place to place
macula a small spot of relatively acute central vision, containing the fovea
Magdalenian a human tool culture that made many types of tools from bone and antler,
some decorated with carvings
magnocellular response a rapid response to visual stimulation that preserves only fuzzy
detail but serves to alert the system to the appearance and location of the stimulus
maintenance rehearsal rote repetition
malleus literally, “mallet”; one of the ossicles of the middle ear
mechanoreceptors specialized sensory receptor cells that react to mechanical forces
medial inner; toward the middle
medial lemniscal system somatosensory neural pathways that run upward to the medulla
of the brain, and then via synapses to primary somatosensory cortex
Meissner’s corpuscles touch receptors below the outer layers of skin, detecting flutter
memory set several items held in memory
memory span the number of items that can consistently be recalled in correct order
memory stores kinds of memory
Merkel’s receptors (or discs) touch receptors below the outer layers of skin, detecting
fine details
metabolism the cellular process by which energy is made available
metacognition the awareness of one’s own cognitive states and processes
metazoa multicellular animals
microblades small stone blades less than 5 cm in length
microcephalic abnormally small-brained
microliths small stone blades with at least three distinct sides
310 Glossary
microvilli tiny projections of cell membrane
minicolumns columns of neurons in the cortex, oriented vertically to the cortical surface
and extending through most of the cell layers
mirror cells neurons that rapidly fire when their possessor observes the actions of others,
and when he or she makes the same motions
missing heritability problem the observation that when single gene effects are cumu-
lated, they fail to account for the full heritability of a behavior or characteristic
mitochondria small structures responsible for energy production in a cell
molecular clock a method of dating based on genetic differences between species
monocular cues depth cues that can be seen by a single eye
monozygotic twins identical twins
motile independently moving
Mousterian a hominid tool culture usually associated with Neanderthals
mutation a copying error within a chromosome resulting in an altered set of instructions
myofibrils chains of protein in muscle fibers that contract when stimulated
natural selection the environmental favoring of traits, improving survival and re-
production
negative hand the outline of a hand held against a rock and painted by blowing pigment
through a tube held by the other
neoteny the retention of juvenile characteristics in adulthood
neural crest a cluster of embryonic cells arranged in ridge-like formations to the sides of
the neural tube
neuromuscular junction the location where a motor neuron synapses onto muscle fiber
neurons nerve cells
New World monkeys monkeys native to the Americas
nocturnal active at night
notocord a supporting rod in chordates, located in front of a hollow neural tube
nucleotide a molecule composed of a nucleobase, a sugar, and a phosphate
occlusion a monocular depth cue in which an object whose image partially blocks another
is judged closer
Old World monkeys monkeys native to Africa, Asia, or Europe
olfactory epithelium a layer of neurons lining the upper portion of the nasal passageway
olfactory sense, or olfaction sense of smell
omnivore an animal that eats both animals and plants
opposable thumb a thumb that can rotate along its long axis, allowing its pad to contact
the pads of other fingers
opsins a family of photopigments
optic flow the experience of objects rushing past in the periphery while the view far ahead
changes much more slowly
optic foramen a small opening in the bone of the eye socket through which the optic
nerve passes
orienting the shifting of eyes, attention, or both toward a source of stimulation
oscula mouth-like openings
ossicles three small bones in the middle ear
Pacinian corpuscles touch receptors, deeply embedded in the skin, that respond to vi-
bration
paleocortex ancient cortex
parietal eye field a location in the parietal lobe of the brain that updates spatial in-
formation in response to movement
Glossary 311
parvocellular response a relatively slow response to visual stimulation that contains
detailed information
pattern mask a stimulus composed of jumbled features that spatially covers another
stimulus
peptides short chains of amino acids
perceptual invariance the ability to recognize an object regardless of physical transfor-
mations of characteristics like position, depth, size, viewing angle, contrast, and texture
Périgordian (called Gravettian outside France) a human tool culture characterized by
backed blades and end-scrapers
perirhinal cortex cortex located in the medial temporal lobe, literally “near the nose”
perisylvian cortex cortex located around the Sylvian fissure
phonological syntax the ordering of meaningless sound elements
phonology language phonetics
phosphenes imaginary points of light
photomotility movement in response to light
photopigments pigments that react chemically to light
phylogeny evolutionary relationships
phytoliths microscopic mineral particles formed by plants
pinna outer ear
place cells neurons that respond to particular locations in the environment
placode a specialized cell cluster, representing a thickening of the ectoderm during ver-
tebrate prenatal development that develops into a structure
planum temporale, or temporal plane a small surface of cortex located lateral and
posterior to Heschl’s gyrus
Platyrrhini literally, “broad-nosed” monkeys, also known as New World monkeys
“pli-de-passage fronto-parietal moyen parietale” (PPFM) a gyrus in the brain that
is buried along the central sulcus, connecting the precentral and postcentral gyri
podomeres leg segments
polydactyly the condition of having more than five digits per limb
population left-handedness (PLH) a predominance of left-handedness in a population
population right-handedness (PRH) a predominance of right-handedness in a popu-
lation
positron emission tomography (PET) a method for imaging brain activity that involves
injecting a radioactive substance into the bloodstream, followed by the detection of
decay products immediately outside of the head
postcranial pertaining to the skeleton below the head
potassium-argon dating a geological clock method that assigns dates according to the
ratio of potassium-40 to argon-40
praxis the ability to conceive, initiate, and complete movement
preadaptation an evolutionary change later built upon by other changes
precision grip the delicate holding of a small object between the index finger and thumb
precuneus the medial portion of area 7
prefontal cortex the forward portion of the frontal lobes
prehensile able to grasp objects
primary representation the ability to mentally represent the world in a realistic, literal way
primary sensory cells neurons with sensors at one end and an axon out the other end
primates an order of eutherians with highly mobile feet and hands, and opposable digits
primitive character a characteristic possessed by the earliest evolving member of a clade
primordial soup the thin solution of chemicals comprising the early ocean
prokaryotes literally, “before kernels”, i.e., cells without nuclei
312 Glossary
prosimians outmoded term for primates “before apes”, consisting of the Strepsirrhini and
tarsiers
prosopagnosia the inability to recognize faces presented visually
protocell a self-replicating compartment enclosing chemical processes
proximal nearer to the core
pseudogenes genes that have become deactivated because of disruptive mutations
pseudoneglect overattention to one side of space due to an intact attentional mechanism
on the opposite side of the brain
Psittacidae the family of parrots
pulvinar a nucleus in the thalamus
pursuit eye movements eye movements that follow a moving object
pyramidal tract a motor tract originating in the precentral gyrus of the brain, that crosses
over to the opposite side of the body; also known as the corticospinal or dorsolateral tract
quadriceps muscles on the front of the thigh that extend it
quadrupedal four-legged; moving on four legs
quorum sensing the ability of some bacteria to detect the presence of increasing numbers
of other bacteria, by sensing a building concentration of chemical excretions
radiation expansion in the number of species
recency effect a memory phenomenon in which the most recent item or items in a list are
recalled better than the items immediately preceding
reentrant connections connections from higher-order cortical areas back to primary
cortex
relative size a monocular depth cue in which the images of two similar objects are
compared and the larger is judged closer
residual brain size the amount of brain over and above that predicted by body weight
retouching secondary flaking along the edge of a stone tool
retrosplenial cortex cortex immediately posterior to the corpus callosum
right-shift theory the theory stating that human handedness is the product of a bell-
shaped distribution in combination with a right-shift allele that is present in some in-
dividuals and not others
robust heavily built
rods a class of receptors in the retina, chiefly responsible for night vision
root hair plexus nerve endings wrapped around the base of a hair
rostral forward
route knowledge knowledge of landmarks and associated turns, used in learning pathways
from one point to another
Ruffini’s endings (or corpuscles) touch receptors, deeply embedded in the skin, that
respond to skin stretching
saccades eye movements toward a source of stimulation
saccule a fluid-filled cavity in the inner ear with sensors that respond to acceleration
sagittal crest a ridge of bone running front-to-back on the top of the skull
savanna grassland with sparse stands of trees
script a contextually dependent series of actions leading to a goal
secondary representation the ability to separate a primary representation from its en-
vironmental reference for hypothetical purposes
secondary sensory cells neurons with a sensory end and a broad synaptic surface on the
other end
semantic dementia a disorder in which use of semantic knowledge is impaired even
though episodic memory is spared
semantic memory memory for facts that make up our knowledge structure
Glossary 313
sensory memory a very short-lived memory trace that preserves much of the physical
form of stimuli
sessile attached, as to the sea bottom
sexual selection mate selection by desirable qualities, e.g., particular colorations or forms
simple cells in the visual system, neurons that perform a feature analysis by representing a
scene in terms of small segments of contours, and that may incorporate color
social learning the acquisition of new behaviors by observing others
Solutrean a human tool culture known for creating the laurel-leaf point through pressure
flaking
somatosensation the sense of touch, or the tactile sense
spatial attention the ability to attend to objects or locations independent of eye position
spatial neglect, or visual neglect difficulty in orienting to objects opposite the side of
a brain lesion
speciation the creation of new species
spike potential a sudden increase in positivity that travels up a neuron’s axon, opening
sodium channels
split time the latest date at which there was any genetic interchange between two species
stapes literally, “stirrup”; one of the ossicles of the middle ear
stem group a group prior to diversification into crown groups
Strepsirrhini strepsirrhines, literally “wet-nosed” primates
striking platform in the making of a stone tool, a small flat surface where a blow landed
stromatolites mats of sediment formed by bacteria
subitizing a perceptual process that rapidly enumerates small numbers of items
superficial layer of V1 the layer of V1 cells closest to the surface of the brain, also known
as layer 1
suprachiasmatic nucleus a nucleus of neurons connected to the ganglion cells of the
retina, involved in maintaining the circadian rhythm
survey knowledge knowledge of how landmarks are configured relative to one another
symbiotic mutually beneficial
symmetrical gait a gait with a movement cycle taking the same length of time for the
forelimbs as for the hindlimbs
sympatric speciation the evolution of new species within an unseparated population
synapsids tetrapods with one opening in the skull behind the eye
syntax, or grammar the rule-based organization of symbols in orders that succeed in
conveying meaning
tactile pertaining to touch
Talairach space a set of X, Y, and Z coordinates allowing the mapping of brain activity
to structures in an “average” brain
tapetum lucidum literally “silvery carpet”; the reflective layer behind the retinas of
certain animals such as cats and dogs
taxa classifications of organisms based on relatedness
tectopulvinar pathway a visual pathway that proceeds from the eye to the superior
colliculus, then to the pulvinar, and finally to the secondary visual areas of the cortex
tensor tympani muscles muscles in the middle ear, connected by a ligament to the
malleus
termite fishing a behavior in which a twig is prepared and then inserted into termite
mounds, allowing the withdrawal of termites
terrestrial living on the ground
tetrachromacy the state of having four types of cones
tetrapods vertebrates with four feet or legs
314 Glossary
theory of mind the ability to ascribe mental and emotional states to others
thermophilic heat-loving
theropods large carnivorous dinosaurs with short forelimbs and large jaws
thoracic vertebrae vertebrae at the level of the thorax or chest
trace fossils fossils of behavior as opposed to physical form
trichromacy the state of having three types of cones
trichromatic vision three-color vision
tuff a layer of rock formed from compacted volcanic ash
umami a meaty or savory flavor
utricle a fluid-filled cavity in the inner ear with receptors that respond to acceleration
ventral bottom
ventral visual stream the visual pathway from brain area V1 to the temporal lobe
Vernier acuity the ability to determine whether two aligned line segments are con-
tinuations of the same line or rather are offset from one another
vertebral canal the opening in the vertebrae through which the spinal cord passes
vertebrates animals with a brain and a vertebral column
vesicles sacs
vestibular sense the sense of balance
visual agnosia the inability to recognize a class of objects presented visually
Visual neglect, visuospatial neglect, or spatial neglect difficulty in orienting to objects
opposite the side of a brain lesion
visual word form area (VWFA) a brain area in or near the occipito-temporal sulcus,
involved in recognizing words presented visually
visuospatial neglect, visual neglect, or spatial neglect difficulty in orienting to objects
opposite the side of a brain lesion
vomeronasal sense a chemical sense that detects pheromones using receptors in the nasal
passages
Wernicke’s area the posterior portion of the superior temporal gyrus implicated in the
decoding of speech sounds
working memory a form of memory that holds and manipulates information over the
short term
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Author Index
Note that names beginning ‘Mc’ are filed as ‘Mac’.
Aerts, P. 157 Beyene, Y. 78

Ahlberg, P. E. 69 Blake, J. 260
Al Omran, Y. 173 Bloch, J. I. 78, 186
Alexander, I. 282 Boccia, M. L. 287
Alexander, R. M. 145 Boesch, C. 182, 221
Alfaro-Almagro, F. 173 Boisserie, J.-R. 78, 144
Allen, C. 279 Boisvert, C. A. 133
Allison, T. 14, 233 Boles, D. B. 215–216, 222
Anderson, J. R. 291 Boyer, D. M. 78
Angeli, R. D. 103 Boyle, E. A. 303
Annett, M. 171 Boyle, E. K. 78, 90
Antonelli, A. 191 Bradshaw, J. 35
Arendt, D. 98, 118 Brandt, A. 32
Argue, D. 88 Brown, J. C. 273
Arshad, S. 289 Brown, P. 88
Arsuaga, J. L. 272 Brumm, A. 78
Asara, J. M. 39 Bruner, E. 223
Asfaw, B. 68, 78 Brunet, M. 78
Astafiev, S. V. 219 Bryden, M. P. 169–171
Athanassiou, A. 69 Bü chel, C. 221
Awe, R. D. 78 Bullier, J. 282
Burger, J. 303
Baddeley, A. 246 Bussey, T. J. 252
Ballarin, C. 289 Bustamante, C. D. 109
Ban, S. D. 221 Butler, R. J. 172
Baragli, P. 288 Buxhoeveden, D. P. 270
Bargalló , A. 174 Byatt, G. 233
Barriel, V. 89 Byrne, R. W. 261, 292
Batzer, M. A. 55
Begun, D. R. 78 Caetano-Anolles, G. 11
Bekoff, M. 279 Call, J. 251, 253
Belger, A. 233 Cameron, D. W. 78
Bemtsen, D. 251 Cantley, L. C. 39
Benazzi, S. 78 Carlson, K. J. 78
Benham, A. E. 186 Cartmill, E. A. 292
Bennett, E. L. 247 Casanova, M. F. 270
Benoit, J. 69 Cavanagh, J. P. 245
Beran, M. J. 285 Chemnick, L. G. 55
Berger, L. R. 78, 81 Churchill, S. E. 78, 81
Bergeret-Medina, A. 144 Clayton, N. S. 252
Bering, J. M. 291–292 Coffing, K. 78
Berner, M. 301 Cohen, L. 275
Bever, T. G. 262 Colagé, I. 218
Author Index 371
Collard, M. 88 Falk, D. 78, 88, 269
Colmenares, F. 253 Fassoulas, C. 69
Colombo, P. J. 247 Faurby, S. 191
Colon, M. R. 251 Faurie, C. 177
Conde-Valverde, M. 272 Fegley, B. 5
Constantino, P. 78 Fernald, R. D. 115, 125
Cook, R. G. 245 Fernandez-Carriba, S. 167–168
Coppens, Y. 187 Field, Y. 303
Corbetta, M. 219 Fisher, S. E. 172
Coulon, O. 177 Fize, D. 212, 231
Cowey, A. 282 Fortin, N. J. 253
Cozzi, B. 289 Fox, E. A. 183
Crow, T. J. 172 Francks, C. 172
Freedman, D. J. 217
Dalmyn, C. K. 186 Freimark, L. M. 39
D’Aoû t, K. 157 Fritzsch, B. 103
Dann, J. C. 172 Furniss, D. 173
Daver, G. 144
Davidson, I. 182 Gabrieli, J. D. E. 221
Davila, A. F. 8 Galliot, B. 97
De Clercq, D. 157 Gallup, G. G. 285–287, 291
De Lillo, C. 237, 246 Gao, Z. 303
de Ruiter, D. J. 78, 81 Garofalo, E. 301
de Waal, F. B. M. 288, 292 Garvin, H. M. 88
Deaner, R. O. 186 Gauchat, D. 97
Dehaene, S. 275 Gaulton, K. J. 303
d’Errico, F. 218 Geffen, G. M. 171
Delezene, L. K. 78, 81 Georgi, J. A. 41
DeLisi, L. E. 172 Ghirlanda, S. 246
Dembo, M. 88 Giacobini, G. 218
Dennett, D. C. 279 Giambrone, S. 203
Denys, K. 231 Gibson, E. K. 8
Derst, C. 95–96 Gierlinksi, G. D. 69
DeSilva, J. 69 Gilad, Y. 108–109, 124
Dias, M. A. 155 Girard, P. 282
DiCarlo, J. J. 232 Givens, S. M. 215–216
Dickinson, A. 252 Golan, D. 303
Dirks, P. H. G. M. 78 Golston, C. 27
Djimdoumalbaye, A. 78 Gómez, J.-C. 261
Dominy, N. J. 99, 109 Gommery, D. 188
Doyon, L. 218 Goodall, J. 182
Dubicka, Z. 69 Goodman, M. 20–21
Duffy, D. L. 171 Gorce, P. 187
Dunbar, R. 128 Gorno-Tempini, M. L. 254
Duncan, J. S. 103 Gowlett, J. A. J. 85
Granato, A. 289
Ebisuzaki, T. 7 Greenfield, P. M. 262
Eichenbaum, H. 253 Grine, F. E. 67
Elkins, W. 221 Grossman, L. I. 20–21
Elliott, K. L. 103 Grove, M. 85
Elliott, M. 78 Groves, C. P. 78
Emery, N. J. 293 Gü ntü rkü n, O. 288
Eng, C. M. 155 Guttmannova, K. 284
Enquist, M. 246 Guy, F. 78, 144
Evans, S. 251
Eyun, S. 108 Haile-Selassie, Y. 78
Halsey, L. G. 145
Fagot, J. 238, 246 Hampton, R. R. 250
Fairen A. G. 8 Han, K. 55
372 Author Index
Hård, T. 110 Kopecky, B. J. 103
Harrington, A. R. 78 Kordos, L. 78
Haun, D. 253 Krachen, C. 290
Hawks, J. 78, 81 Kreiman, G. 232
Hayden, B. 189 Kubo, D. 78
Hayes, J. M. 26 Kupsky, W. J. 76, 289
Hecht, E. E. 290 Kurokawa, K. 7
Heffner, R. S. 127 Kurniawan, I. 78
Hewitt, G. P. 271
Hieshima, G. B. 26 Lacalli, T. C. 106–107, 119, 140–141
Higgins, R. 145 Laird, M. F. 88
Hildebolt, C. 78, 88 Lamme, V. A. F. 282–283
Hjelm, M. 210 Lancet, D. 108–109, 124
Hobaiter, C. 261 Laska, M. 110
Hocking, J. 254 Latash, E. M. 167
Hoffman, J. N. 99 Latimer, B. 68
Hoffman, M. L. 251 Laval, S. H. 172
Hoke, K. L. 125 Le Vraux, E. 218
Holt, B. 301 Leask, S. J. 172
Hopkins, A. M. 167 Lee, D. W. 247
Hopkins, W. D. 167–169, 177, 236–237, 264, Lefebvre, L. 289
267, 290 Leh, S. E. 280
Hostetter, A. 167–168 Lehmann, T. 78
Huang, C. H. 55 Lemieux-Lefebvre, S. 289
Hubel, D. 227–228, 230 Leonard, W. R. 145
Hung, C. P. 232 Lewis, A. 251
Hunt, K. D. 57 Li, D. 110
Hupé , J.-M. 282 Lieberman, P. 270, 273–274
Huxley, T. H. 38 Lihoreau, F. 78
Likius, A. 144
Ida, Y. 169–170 Lind, J. 246
Iltis, D. 197 Lise, M. 103
Liszkowski, U. 261
Jahan, I. 103 Litaker, M. 270
James, W. 282, 283 Liu, G. 20–21
Janmaat, K. R. L. 221 Liu, Y. 284
Jatmiko, Y. D. 78, 88 Lockley, M. G. 69
Jenkins, J. 32 Loftus, J. 172
Jerison, H. J. 99, 128 Logan, G. A. 26
Ji, Q. 41 Lomber, S. G. 282
Johanson, D. 90 Long, G. M. 241, 242
Johnson, V. 186 Lorenzo, C. 272
Jones, S. 192 Lovejoy, C. O. 68, 78
Lucas, P. W. 109
Kaifu, Y. 78 Luo, Z.-X. 41
Kaiser, E. 303 Lurz, R. 290
Kappelman, J. 78
Karschin, A. 95–96 McCarthy, G. 14, 233
Kayser, M. 303 McCarthy, P. 173
Kendrick, D. F. 245 Macchiarelli, R. 144
Kersken, V. 261 MacGregor, L. 267
Kibii, J. M. 78 McGrew, W. C. 181–182
Kim, K. M. 11 McHenry, H. M. 78
King, W. 84 McKay, D. S. 8
Kirk, E. C. 127, 128, 208 Mackaye, H. T. 144
Kirsanow, K. 303 McKeever, W. F. 172
Knutsen, T. A. 212 MacLarnon, A. 271
Kö hler, W. 180 McManus, I. C. 171
Kono, R. T. 78 McNutt, E. 69
Author Index 373
Maffacioli, T. B. 103 O’Connell, B. 32
Maglieri, V. 288 Orban, G. A. 231
Mahovetz, L. M. 290
Mandeville, J. B. 212 Pä ä bo, S. 108–109, 124
Mandler, G. 214 Palagi, E. 288
Mandre, S. 155 Pan, N. 103
Manley, G. A. 104 Patterson, K. 254
Marchant, G. H. 76, 289 Payne, B. R. 282
Marchi, D. 144 Pearce, E. 128
Marchini, J. 173 Pei, M. 284
Mareno, M. C. 167, 177 Perdue, B. M. 285
Marino, L. 289 Petito, L. A. 262
Marletaz, F. 32 Peuskens, H. 231
Marlow, H. 98 Phillips, J. B. 215–216
Martin, N. G. 171 Phillips, K. A. 167
Martin, R. 192 Phillips. M. 39
Martin, R. D. 76 Phillipson, L. 174
Martin-Ordas, G. 253 Pilbeam, D. 70, 192
Martínez, I. 272 Pilcher, D. 167–168, 267
Maruyama, S. 7 Plotnik, J. M. 288
Marzke, M. W. 188 Pobiner, B. L. 174
Marzke, R. F. 188 Poggio, T. 232
Maureille, B. 218 Pope, S. 177
Medland, S. E. 171 Posner, M. I. 283
Meguerditchian, A. 177 Poss, S. 167–168
Meldrum, J. 69 Postma, A. 209
Melillo, S. M. 78 Pouydebat, E. 187
Menzel, C. R. 251 Povinelli, D. J. 203, 291–292
Merker, B. 283 Povinelli, M. 289
Michelli, A. 254 Preuss, T. M. 290
Michie, P. T. 233 Price, C. J. 254
Miljkovic-Licina, M. 97 Prior, F. 78, 88
Miller, E. K. 217 Prior, H. 288
Miller, G. A. 245 Pritchard, J. K. 303
Mishkin, M. 281 Przeworski, M. 108, 124
Misiura, M. 167, 177 Ptito, A. 280
Moffat, S. D. 221 Puce, A. 14, 233
Monaco, A. P. 172
Montag, A. G. 99 Quam, R. M. 272
Moore, B. R. 241 Queffelec, A. 218
Morwood, M. J. 78, 88
Mosquera, M. 174 Radovcic, D. 88
Moussa, A. 144 Ramsey, N. F. 209
Mullen, K. T. 280 Rantala, M. J. 197
Murofushi, K. 216–217 Ray, D. A. 55
Raymond, M. 177
Nakamura, R. K. 281 Reaux, J. E. 203
Nasir, A. 11 Reiss, D. 288
Neggers, S. F. W. 209 Renner, S. S. 22
Nekoulnang, C. 144 Resnick, S. M. 221
Nelissen, K. 231 Reynolds, V. 182
Nelson, T. O. 284 Rhodes, G. 233
Ng, M. 173 Richardson, A. J. 172
Nieder, A. 217 Rightmire, G. P. 78
Niedzwiedzki, G. 69 Rivas, E. 260–261
Nishida, T. 182 Roberts, E. M. 78
Niskanen, M. 301 Roberts, R. G. 78
Noppeney, U. 254 Robertson, M. L. 145
Norlén, E. 110 Rodriguez, I. A. 251
374 Author Index
Rogers, A. R. 197 Simakov, O. 32
Rogers, T. T. 254 Singh, D. K. 155
Rokhsar, D. S. 32 Sitompul, A. F. 183
Romanek, C. S. 8 Sjöström, D. 110
Rosa, M. 272 Sladek, V. 301
Rosenzweig, M. R. 247 Smith, J. D. 284–285
Ross, C. F. 208 Smith, K. 78, 88
Roy, E. 270 Snyder, A. Z. 219
Rue, J. 172 Sol, D. 289
Ruff, C. B. 145, 301 Soldati, A. 261
Ruhlen, M. 274 Spinozzi, G. 237
Russell, J. L. 169, 264 Srinivasan, S. 106
Russon, A. E. 259 Stanford, C. B. 147, 150
Rutschmann, F. 21 Stanley, C. M. 219
Ryan, T. M. 78 Stein, J. F. 172
Steudel-Numbers, K. L. 145
Sakata, H. 222 Stevens, C. F. 106
Sakitt, B. 241–242 Strait, D. S. 67
Salvi, V. 237 Su, Y. 284
Sanchez, I. C. 251 Suda, K. 7
Sanders, R. J. 262 Sugiyama, Y. 182
Sands, S. F. 245 Summons, R. E. 26
Santiago, H. C. 245 Sutikna, T. 78, 88
Santosh, M. 7 Suwa, G. 68, 78
Saptomo, E. W. 78, 88 Switala, A. E. 270
Sarmiento, E. 69
Sasaki, Y. 212 Tabajara, C. C. 103
Sato, N. 222 Taglialatela, J. P. 264
Savage-Rumbaugh, E. S. 262 Taira, M. 222
Sawaki, Y. 7 Tanaka, Y. L. 222
Schaefer, L. 5 Telis, N. 303
Schaeffer, J. A. 264 Terrace, H. S. 262
Schapiro, S. J. 167, 169, 177 Theall, L. A. 203
Schmid, P. 78, 81 Thomas-Keptra, K. 8
Schmid, V. 132 Timpson, A. 303
Schoonaert, K. 157 Tocheri, M. W. 78
Schroeder, L. 88 Tommasini, S. M. 155
Schulze-Makuch, D. 8 Tomonaga, M. 238
Schwartz, B. L. 250–251 Tootell, R. B. H. 212
Schwarz, A. 288 Tosches, M. A. 98
Schweitzer, M. H. 39 Toth, N. 173–174
Scopa, C. 288 Tsao, D. Y. 212
Scott, J. E. 88
Seipel, K. 132 Uddin, M. 20–21
Semaw, S. 189 Unterlä nder, M. 303
Semendeferi, K. 200–201 Uomini, N. T. 174
Semenov, S. A. 174
Senut, B. 69, 188 van den Bergh, G. D. 78
Serrrano, P. A. 247 Van der Lubbe, R. H. J. 209
Setiyabudi, E. 78 Van Elsacker, L. 157
Shaw, S. H. 172 Van Essen, D. 231
Shebo, B. J. 214 Van Essen, D. C. 219
Shelton, A. L. 221 Van Lawick-Goodall, J. 180
Shields. SW. E. 284 van Schaik, C. P. 183, 186
Shillito, D. J. 291 Vanduffel, W. 212, 231
Shoshani, J. 76, 289 Vazzana, A. 78
Shulman, G. L. 219 Velez, A. D. 272
Silcox, M. T. 78, 186 Venkadesan, M. 155
Silvestro, D. 191 Vereecke, E. 157
Author Index 375
Walker, C. S. 78, 81 Wolpert, L. 203
Wang, H. 55 Wood, B. 144
Washburn, D. A. 236–237, 284 Wood, B. A. 78, 90
Weiller, C. 221 Wooding, S. 197
Werdkin, L. 191 Wright, A. A. 245
Wesley, M. J. 167–169 Wright, M. J. 171
White, C. R. 145
White, S. 85 Xing, J. 55
White, T. D. 68, 71, 78 Xu, G. 284
Whiten, A. 182
Whittey, E. 301 Yang, T. 103
Wiberg, A. 172–173 Yapunich, G. S. 78
Wible, J. R. 41 Yawar, A. 155
Widianto, H. 89 Yuan, C.-X. 41
Wiebe, V. 108, 124 Yue, J.-X. 32
Wiesel, T. 227–228, 230
Wilde, S. 303 Zahnle, K. J. 5
Wildman, D. E. 20, 21 Zeitoun, V. 89
Williams, M. F. 76–78, 186 Zhang, J. 110
Wittbrodt, J. 118 Zhang, J.-P. 41
Wolbers, T. 221 Zipfel, B. 69
WoldeGabriel, G. 78 Zollikofer, C. 78
Subject Index
Locators in bold refer to tables and those in italics to figures.
Acanthostega 33–34, 105, 133 Australopithecus aethiopicus 75–76

Acheulean tools 192, 193, 194, 199 Australopithecus afarensis: arms and hands 153;
acritarchs 17 bipedalism 145; fossil record 71–73, 72, 74;
acuity (vision) 126–127, 206–208 human evolution 90; legs and feet 154–155;
Aegyptopithecus 53, 54 “Lucy” 71, 72; parietal lobe 223;
aethiopicus; see Australopithecus aethiopicus reconstruction 75
afarensis; see Australopithecus afarensis Australopithecus africanus: arms and hands 153; fossil
africanus; see Australopithecus africanus record 74–75; human evolution 90; hyoid 270
agrammatism 264 Australopithecus anamensis 71, 90, 153
Ahrensburgian tools 198 Australopithecus garhi: fossil record 74; human
allocentric frame of reference 209, 210 evolution 90; tool use 189, 190
allopatric speciation 14–15 Australopithecus sediba 76, 154, 269
amniotes 35–36, 37, 134–135 autosomal genes 82, 171–172
amphibians 34, 35
amphioxus 26–27, 28, 98, 106, 111, 119, 140 bacteria: chemical signaling 95, 96; locomotion in
anamensis; see Australopithecus anamensis 131; origins of life 7, 8, 10–12, 16, 24
anatolepis 30, 31 bacterial flagella 131
angular gyrus 275–276 balance 100–102, 296
anterior inferotemporal cortex 226 basilar membrane 102–104, 296
anthropoids, tarsier-anthropoid divergence 48 Bilateria 24, 98, 118, 119, 132–133
ape divergences 56–61 binocular convergence 211
apes: bipedalism 148–150; the first ape 298–299; the binocular cues 210
first great ape 299; handedness 168–169; knuckle binocular disparity 211
walking 137; language use 257, 259–260, binocular field of view (BFOV) 211
262–265, 276; referential pointing 292; self- biomineralization 30
recognition 287–288; tool use 180–181; vocal bipedalism 144; causes of 144–150; consequences of
tract 273–274 150–158; the first hominin 299; “Lucy”,
arboreality 81, 136–138 Australopithecus afarensis 71, 72
archaea 6–7, 11, 24, 131 birds: as dinosaurs 38; encephalization 289–290;
archaeological evidence: cave art 175; evolution of long-term memory 252, 253; self-recognition
language 274; handedness 173–175; quantity 288; short-term memory 245–246; theory of
representation 217–218 mind 293; tool use 184, 185
Ardipithecus 67–68, 68 “black smokers” 6–7
Ardipithecus ramidus 67, 71, 90, 156 blindsight 280–281
art, in caves 175 body size: evolutionary trends 88–89; primates and
artiodactyls 23–24 hominins 137; spatial perception 211;
association, in memory 240 see also brain-body size relationship
attention 219–220, 282–284 boisei 75–76
auditory pathways 281 bone strength 301–302
auditory sense 102–106; deaf hearing 280–281; the bonobos; see chimpanzees
first eutherian 297; hearing sensitivity 272; brachiation 51, 137
localization thresholds 127 the brain: evolutionary changes to the eye 127–129;
Aurignacian tools 195 language 263–268; lobes 100; memory 250;
Subject Index 377
navigation 221–222; olfactory neural pathways climate change, influence on bipedalism 146
106, 107; perceptual information 220–221; Clovis tools 198–199
planning and use of tools 200–204; praxis cnidarians 17, 32, 97, 114, 118, 132, 240, 295
163–166, 175–177; recognizing location coalescence time 82
208–209; spatial perception 223; tactile neural cognition: Homo habilis 78–79; metacognition
pathways 99, 100; “what” and “where” pathways 284–285; navigation 221–222; pattern
208, 208, 212, 227; see also Brodmann areas recognition 226–238; planning 200–204; praxis
brain-body size relationship: birds 289–290; 163–166, 175–177; self-recognition 285–290,
evolutionary trends 88–89; the first human 300; 300; social learning 183–184; theory of mind
primates and hominins 76–79, 78; self- 291–293; tool use 191; see also the brain
recognition 289, 289–290; tool use 185–186, 186 Colobinae 63
brain size, in primates: parietal lobe 223; planning color vision 119–125, 280
200; tool use 184–186 composite tools 194
breathing, and language 271 conditioning 240–241
Broca’s area 176, 247, 263–264, 266, 278, 301 cones (eyes) 119–125, 126, 127, 242
Broca’s cap 269–270 consciousness 279; attention 282–284;
Brodmann areas 176; auditory sense 281; causation metacognition 284–285; self-recognition
204; language 263–264; memory 246–247, 248; 285–290; sensory awareness 279–282; theory of
pattern recognition 227; planning and the rise of mind 291–293
area 10 200–203; spatial perception 209, 210, contralateral organization, origin of 139–142
218, 219, 220, 221 cooking hypothesis 109
cornea (eyes) 117, 125–126, 208, 297
Cajal’s proposal 139–142 cortical magnification factor 206
Cambrian explosion 24–25 corticospinal tract 138
capuchins: metacognition 285; pattern recognition cranial nerves 109
237, 237; self-recognition 287; tool use 185–186 creativity, and left handedness 177
carbon dioxide levels, vomeronasal sensory crown group 22–23
system 111 cultural change 301–303
carnivore extinctions, East Africa 191 culture: 182-184 192, 195, 197–198
Carpolestes simpsoni 45 cutaneous nerves 99
carrying, as advantage of bipedalism 147 cyanide 6
catarrhines, platyrrhine-catarrhine divergence 48–56
cave art 175 Darwin, Charles 14, 23–24, 70
cell membranes 95 dating, of fossils 19–23, 27
central nervous system (CNS) 111 deaf hearing 280–281
Cercopithecinae 63; see also macaques deception behaviours 292–293
cerebellum 165 demosponges 17
chemical reaction, for vision 114 Denisovans 84–85
chemical senses 95; early sensing 95–96; oxygen and deoxyribonucleic acid (DNA): beginnings of life 8;
carbon dioxide levels 111; smell 106–109; taste mitochondrial DNA 90–91; molecular clocks
109–110 19–22; structure 4; transition to DNA world 10
children: gesture 261; language 263, 265; depth, perception of 210–212
metacognition 284; self-recognition 286 derived characters 23–24
chimpanzees 62, 63; bipedalism 147–148; dexterity 188; see also tools, use by humans
handedness 167–168, 170, 171; human ancestral diapsids 37, 37–41
line 60–61; and human evolution 65, 269; dinosaurs 18, 38–40, 133, 134
language 262–263, 265, 269; pattern recognition dizygotic twins 171
237–238; population right-handedness (PRH) DNA; see deoxyribonucleic acid
176; self-recognition 285–286; spatial perception dolphins 288, 292
221; taste 110; theory of mind 291; tool use dorsal visual stream 208, 208, 212
180–181, 182–184, 189; tripedal walk 157 dorsolateral tract 138
choanoflagellates 96
chordates 26–27, 29, 31–32, 99, 103, 112, 118, 119, ears: auditory sense 102–106; origin of the ossicles
132, 140, 295, 296 105–106; sensitivity for language 272; vestibular
circadian rhythm 118, 119 sense 101–102
cladistics 23–24 egocentric frame of reference 208–210
cladogram, human ancestral line 67 elaborative rehearsal 250
classical conditioning 240 elephants 185, 288, 289, 292
clay surfaces 6 encephalization quotient (EQ): evolutionary trends
378 Subject Index
88–89; the first human 300; primates and ganglia 32
hominins 76–79, 78; self-recognition 289, garhi 74, 90
289–290; tool use 185–186, 186 gaze (theory of mind) 291–293
endocasts 200, 201, 223 gene frequency studies 302
endothermy 40 genetics: descent with modification 13; horizontal
Eomaia 40–41, 41 gene transfer 11; mitochondrial DNA 90–91;
Eosimias 48, 49, 62 molecular clocks 19–23; natural selection 13–14;
episodic memory 250–253 population right-handedness (PRH) 171–173;
erectus; see Homo erectus speciation 14–15; transition to DNA world 10
Euglena 114, 206 geniculostriate pathway 280, 280
eukaryotes 10–12, 16, 24, 25–26, 95 geological clocks 19
eumetazoa 17 gesture 261, 292
eutheria 40–41; the first eutherian 296–297 gill arches 33
evolution: Cambrian explosion 24–25; descent with global precedence effect 234, 236
modification 13; how life began 3–9; of language gnostic cells 231
275; natural selection 13–14; one-celled life goals 199–200, 202, 221
10–13; as random process 15; tree of life 23–24, Gona tools 189–191, 190
25–26; workings of 13–15; see also human gorillas 60, 61; handedness 169; knuckle walking
evolution 137; memory study 251; self-recognition 287;
extrapyramidal tract 139 tool use 181
eye movements 218, 219 grammar 261–263, 264
eyes: and the brain 127–129; color vision 119–125; grandmother cells 231–232
evolution of 114–119; genetic basis 117–118; human grasping 220
ancestral line 115–117, 116, 118; light detection Gravettian tools 195
206; night vision 125–126; types 115–116 “great denudation” 197–198
grid cells 209
face recognition 233–234, 239 grip: hominid tool use 299; primate tool use
factor analysis 167–168, 169, 170 187–189
fatty acids 9–10 gustation 109–110
feature analysis 227–228, 230 gustatory pseudogene formation 110
feet 154–156, 155
femurs 145, 146 habituation 240
figure-ground segregation 229–230 hagfish 100, 109, 119
fingers 81, 153, 188 hair follicle receptors 98, 99, 103–104
fire, evidence in hominid cultures 198 hallux 155, 156
fish: 33, 34, 103, 133, 185; consciousness 253, 288; Hamburgian tools 198
movement 30, 35; vision 199 hammers, use by primates 182
flagella 17 handedness: archaeological evidence 173–175;
flagellum-propelled bacteria 131 components of human handedness 169–170;
flatworms 132, 240–241, 244, 295 genetic foundations 171–173; left-handedness
floresiensis; see Homo floresiensis 167, 177–178; population left-handedness (PLH)
footprints (trackways) 69, 71, 73, 155 167; population right-handedness (PRH)
foraging, and bipedalism 146, 150 166–177; reasons for PRH 175–177
fossil record 18, 23–24 haplorhines: eye and brain 128–129; strepsirrhine-
fossils: dinosaurs 38–40; formation 18; as geological haplorhine divergence 45–47, 135–136
clocks 19; handedness 173–174; hominids 65, hearing; see auditory sense
66–87; molecular clocks 19–23; vision, evolution helping behaviours 292–293
of 128 hemisphere lateralization 209–210
fovea 126–127, 128 Heschl’s gyrus 265
FOXP2 gene 270, 301 heuristics 203
frames of reference 208–209, 222 hippocampus 209, 253
frequency selectivity (hearing) 104–105 “The Hobbit” 86, 88; see also Homo floresiensis
frontal eye field 219 homicide rates, left-handedness 177–178, 178
functional magnetic resonance imaging (fMRI) hominin artefacts; see archaeological evidence
213, 246 Hominin phylogeny 89
hominins: bipedalism 144–158; the first hominin
gait: amniotes and mammals 134–135, 136; bipedalism 299–300; hand dexterity 188; handedness 170;
157–158; primates and hominins 136–137 origins of motion 135–138; planning 199–204;
galagos 46, 210, 220 see also human evolution
Subject Index 379
Homo antecessor 84–85 knuckle walking 137–138
Homo, emergence of 76–80
Homo erectus 79–80; fire use 198; pelvis 151; right- lactase persistence 302
handedness 173; size trends 88, 89 lampreys 100, 109, 119
Homo ergaster 79, 79, 88, 198 lancelet; see amphioxus
Homo floresiensis 86–87, 86–87; brain mechanisms language 257; the first modern human 301; frontal
200, 201; language 269–270; size trends 88 brain areas 263–265; grammar 261–263, 264;
Homo georgicus 80 hominin evolution of 269–276, 277; perisylvian
Homo habilis: cognition 78–79; handedness 173; brain areas 265–268; in primates 257, 258–260,
language 267, 269; movement 156; parietal lobe 262–265, 266–267, 276
223; phylogeny 90; size trends 88; tool use laryngeal motor cortex (LMC) 263
188, 190 larynx 270, 273–274
Homo heidelbergensis 80, 80; ears 272; handedness lateral line system, in fish 100
174–175; hyoid 271; phylogeny 89; size trends 88 lateral occipital complex (LOC) 231, 232–233
Homo luzonensis 87 lateral temporal cortex 254–255
Homo naledi 81, 88 left angular gyrus 275–276
Homo neanderthalensis 81–85, 83; handedness left-handedness 167, 177–178
174–175; interbreeding with Sapiens 85; left visual field (LVF) 215, 216, 222
thorax 150 legs 154–156
Homo sapiens 80; emergence of 81; evolution of the lemurs 46
parietal lobe 223; the first modern human lens (eyes) 115, 117, 119, 208
300–301; fossil record 81; handedness 175; Levallois technique 193, 194
interbreeding with neanderthalensis 85; vocal tract life, beginning of: DNA world 10; how life began
274; see also human evolution 3–9; membranes and metabolism 9–10; one-
horizontal gene transfer 11 celled life 10–13; workings of evolution 13–15
howler monkeys 54, 108, 109, 124–125 light sensitivity 125–126; see also vision
Hox genes 31–32 limb changes 134–135
human evolution: consciousness 279; cultural change lipids 9–10
301–303; defining humans 65; evolutionary pruning localized processes, pattern recognition 226, 227
90–91; evolutionary trends and connections 87–90; location, perception of 206–210
eyes 115–117, 116, 118; the first human 300; first locomotion 131, 145; see also motion
(Miocene) hominins 66–70; the first modern human Lomekwian tools 189, 204, 205
300–301; hand dexterity 188; of language 269–276, long-term memory 250–255
277; the missing link 70; the parietal lobe 223; “Lucy”, Australopithecus afarensis 71, 72
Pliocene hominins 70–75; early Pleistocene lungs 271
hominins 75–80; middle and late Pleistocene
hominins 80–87; the senses 95; short-term memory macaques 210, 213, 217, 234, 268, 281, 285, 287
246–247 Magdalenian tools 197, 197
hydrogen cyanide (HCN) 6 magnocellular response 243–244
hydrogen ions 95–96 maintenance rehearsal 250
hydrothermal vents 6–7 mammals: balance 101–102; early mammals 40–41;
hyoid 270–271 later mammals 43–44, 61–64; olfactory genes
107–108; origins of motion 134–135; parasites on
Ichthyostega 133 43; pattern recognition 230; platyrrhine-
inferior parietal cortex 267–268, 268, 298 catarrhine divergence 48–56; strepsirrhine-
inferotemporal (IT) cortex 226, 231, 232–233 haplorhine divergence 45–47; tarsier-anthropoid
intermediate-term memory 247–248, 249 divergence 48; tool use 185; see also primates
interorbital distance 211 mark test (self-recognition) 287–288, 290
intraparietal sulcus 166, 238 mechanical senses 95; balance 100–102; early
ions, transport of 95 sensing 95–96; hearing 102–106; joint position
island dwarfism 88 and muscle tension 111; touch 96–99
mechanoreceptors 96–98, 295
jaws 33, 272–273 Meissner’s corpuscles 98, 99
joint position 111 membranes 9–10
Juramaia 40 memory 240–241; long-term 250–255; sensory
juvenile-led innovation 183 241–244; short-term 244–249
memory set 245
kinesthetic sense 111 memory span 244–245
knappers 173–174 Merkel’s cells 98, 99
380 Subject Index
metabolism 3–4, 9–10 nocturnal animals 45, 47, 123–124, 126
metacognition 284–285 nuclear geyser system 7
metazoa: emergence of 13; origins of motion numerosity curves 214, 214, 216, 217
132–133; vision 114–115, 295
Miocene hominins 66–70, 78 object recognition 231–238
mirror cells 164, 176, 264, 269 occipital lobe 223
mirror-image recognition 258, 285–291 occipito-temporal cortex 233, 275
missing heritability problem 173 occlusion 210–211
the missing link 70 Old World monkeys 55–56, 55–56; divergence
mitochondria 12 from human ancestral line 63; handedness
mitochondrial DNA 90–91 176–177; olfactory sense 108, 109, 111; pattern
mitochondrial Eve 91, 92 recognition 237–238; self-recognition 287; tool
molecular clocks 19–23, 90–91, 270 use 187; vision 124
monkeys: chemical senses 111; early primates 44–45, Oldowan tools 189–191, 192, 204
46; figure-ground segregation 229–230; olfactory bulbs 107, 297, 298
handedness 176–177; metacognition 284–285; olfactory genes 107–108
olfactory sense 109; pattern recognition 237–238; olfactory pseudogenes 108–109, 124
population right-handedness (PRH) 175–176; olfactory sense 106–107
self-recognition 287; sensory awareness 282; one-celled life 10–13
short-term memory 245; tool use 185, 187; vision opposable thumbs 45
124–125; see also individually named species optic flow 212
monocular cues 210 optic nerves 127–128, 211, 298
monozygotic twins 171 orangutans 59, 60; handedness 168; referential
motion: amniotes and mammals 134–135; pointing 292; tool use 183, 187
bipedalism 144–158; the first eutherian 297; the orienting, spatial perception 218–220
first primate 297; metazoans 132–133; neural origins of life; see life, beginning of
mechanisms of movement 138–139; origin of Orrorin 68–69
contralateral organization 139–142; origins of ossicles 105–106, 296–297
131; perception of 212–214; praxis 163–166;
primates and hominins 135–138; single-cell Paleolithic 174–175, 192, 195
organisms 131; tetrapods 133–134, 296 paleontology 19–22
motor neurons 138 parasites, living on mammals 43
motor patterning 156–157 parietal cortex 283–284
Mousterian tools 194 parietal eye field 218–219
movement; see motion parietal lobe 164–165, 210, 219, 221–222, 223, 298
movement-related brain areas 163–166 parvocellular response 243–244
multicellular organisms 17–18; Cambrian explosion pattern mask 243–244
24–25; fossil formation 18; geological clocks 19; pattern recognition 226; features and contours
molecular clocks 19–23; tree of life 23–24, 25–26 227–230; general forms 230–231; localized
muscle tension 111 processes 226, 227; object classes 233–238;
mutations 13–14, 302 objects 231–233; other processes and areas 238
Myllokunmingia fengjiaoa 30, 31 pelvis 151, 154
perceptual invariance 232
naledi 81, 88 perirhinal cortex 238, 254–255
natural selection 13–14 perisylvian brain areas 265–268
navigation, spatial perception 220–222 phonology 266
Neanderthals; see Homo neanderthalensis photomotility 114
neoteny 27 photopigments 114
neural crest 32 photosensitive cells 116
neural mechanisms of movement 138–139 phylogeny: human evolution 89; short-term
neuromuscular junction 138 memory 246
neurons: origin of 97–98; primary and secondary phytoliths 193–194
sensory cells 111; tactile neural pathways 99 pigmentation 302–303
New World monkeys 49–55, 50–54; divergence place cells 209
from human ancestral line 62–63; metacognition planning, and tool use 200–204
285; olfactory sense 108, 109; pattern recognition planum temporale 266–267
237–238; sensory receptors 111; tool use 185, platyrrhine-catarrhine divergence 48–56
187; vision 124–125 Pleistocene: early hominins 75–80, 78; middle and
night vision 125–126 late hominins 78, 80–87
Subject Index 381
pli-de-passage fronto-parietal moyen parietale referential pointing 292
(PPFM) 177 (∗res here) representational capacity (language) 257–261
Pliocene hominins 70–75, 78 retinas (eyes) 119–125, 122, 123, 126, 127
pointing 182, 292 retrosplenial cortex 221
population left-handedness (PLH) 167, 299 ribcage 150, 153
population right-handedness (PRH) 166–169; ribonucleic acid (RNA): beginnings of life 3, 6–7, 8,
archaeological evidence 173–175; components of 9–10; structure 4
human handedness 169–170; genetic foundations right shift theory 171–172
171–173; reasons for PRH 175–177 right visual field (RVF) 215, 216, 222
positron emission tomography (PET) 213, 246 RNA; see ribonucleic acid
postcentral gyrus 99, 100 robustus 75
posterior inferotemporal cortex 226, 227 rods (eyes) 119–125, 126, 127, 242
potassium-argon dating 19 route knowledge 220–221
potassium ions 95 running 145, 150, 156
praxis 163–166, 175–177
precision grip 187 saccades 218
prehensile tails 51 Sahelanthropus 66, 66–67, 144
premotor cortex 163–164, 164 scripts, tool behaviours 199
primary auditory cortex 281, 281 secondary representation (language) 258–259
primary motor cortex 164, 165, 175 secondary sensory cells 111
primary representation (language) 257–258 sediba 76
primary sensory cells 110–111 self-awareness 291–293
primates: ape divergences 56–61; early primates self-inspection 286, 290
44–45, 46, 62; emergence of 78; figure-ground self-recognition 285–290, 300
segregation 229–230; the first primate 297; semantic memory 250, 254–255
handedness 167–169; language in 257, 258–260, the senses: balance 100–102; common trajectories in
262–265, 266–267, 276; long-term memory mechanical and chemical sensing 110–112; early
251–253; metacognition 284–285; origins of sensing 95–96; hearing 102–106, 127; human
motion 135–138; pattern recognition between evolution 95; nine “firsts” 296–301; other
species 234, 236–238; platyrrhine-catarrhine mechanical and chemical senses 111; smell
divergence 48–56; self-recognition 285–288; 106–109; taste 109–110; touch 96–99;
short-term memory 245, 246–247; strepsirrhine- see also vision
haplorhine divergence 45–47; see also individually sensory awareness 279–282
named species sensory memory 241–244, 242
primitive characters 23–24 sequencing (ordering) 175, 182, 199, 264, 269
principle of proper mass 128 short-term memory 244–249
problem solving 204, 246 single-cell organisms 131
Proconsul 56–57, 57–58 skin color 302–303
prokaryotes 10–11 skin receptors 98
prosopagnosia 233–234 skull shapes 89, 151
Proto-World language 274–275 smell 106–109
pulvinar 280 social learning 183–184
pursuit eye movements 218 sociality: self-recognition 290; theory of mind
pyramidal tract 138 291–293
Solutrean tools 195, 196
quadriceps 154–155 somatosensation 96–99
quadrupedalism 39, 134; of primates 57, 66, space, beginnings of life 7–8
136–137, 145, 157 spatial attention 219
quantity, perception of 214–218 spatial frequency analysis 227–228
spatial perception 206; depth 210–212; evolution of
radioactivity 7 the parietal lobe 223; independence of spatial
ramidus; see Ardipithecus ramidus processes 222; location 206–210; motion
rat studies: long-term memory 253; spatial 212–214; navigation 220–222; orienting
perception 209, 211; tactile neural pathways 99 218–220; quantity 214–218; reaching and
reaching 220; handedness 167–168, 175 grasping 220
reaction time (RT) 214, 216, 216, 245 spears; see weapons
reading, evolution of 275–276 speciation 14–15
recency effect 245–246 speech 264–266, 269–270, 272
reentry (sensory awareness) 282 spinal column 150, 152
382 Subject Index
split time 82 grip 187–189; the first great ape 299; Gona and
sponges 17, 97, 118, 132 Oldowan tools 189–191; great apes 180–181; later
stem group 22–23 tools 191–199; worked stone tools 189
stone tools 189–191 touch 96–99
strepsirrhine-haplorhine divergence 45–47, 135–136 Toumai 66, 66–67, 144
striking platforms 173 trace fossils 132
stromatolites 12, 12 Transcranial Magnetic Stimulation (TMS) 283–284
subitizing: in humans 214–216; in other primates tree of life 23–24, 25–26
216–217 trichromacy 122–125
superarchaics 84–85
supplementary motor area 163–164, 164 ventral visual stream 208, 209, 275, 298
survey knowledge 220–221 Vernanimalcula 17–18
Sylvian fissure 266, 267 Vernier acuity 206–207, 207
symbolic representation 259 vertebral canal 271
sympatric speciation 14–15, 150 vertebral column 150, 152
synapsids 37, 37–41 vertebrates, evolution of 30, 41–42; amniotes
35–36; early vertebrates 30–33; eyes 119,
tactile neural pathways 99 122–123; the first vertebrate 296; mechanical and
tails, use in motion 133, 134 chemical sensing 111; synapsids and diapsids
tamarins 237 37–41; tetrapods 33–35
tapetum lucidum 126 vestibular sense 100–102
tarsier-anthropoid divergence 48 viruses 11
tarsiers 48 vision 114; acuity 126–127; blindsight 280–281;
taste 109–110, 297 color 119–125, 280; contralateral organization
taxon, age of 22–23 139–142; evolution of eyes 114–119;
tectopulvinar pathway 280, 280 evolutionary changes and the brain 127–129; the
teeth 31, 41, 53, 66, 148, 173 first ape 298; the first eutherian 297; and memory
Teilhardina asiatica 211 241–242; night 125–126; see also spatial
temporal cortex 223, 265, 270 perception
temporal lobe 265, 268–269 visual agnosia 233–234
tensor tympani muscles 103 visual system changes 32
termite fishing 169 visual word form area (VWFA) 275–276
tetrachromacy 122–123 visuospatial neglect 219
tetrapods 33–35; the first tetrapod 296; olfactory vocabulary 259–261, 277–278
genes 107; origins of motion 133–134 vocal tract 273, 273–274
Thatcher illusion 234, 235 vomeronasal system 111
theory of mind 203, 291–293
thermoregulation 146–147 walking; see bipedalism
thoracic canal size 271 weapons 147–148, 150, 181, 188, 194, 198–199
thoracic vertebrae 271 Wernicke’s area 265, 266, 266, 270, 278
thorax 150 Westlothiana lizziae 36
thumbs 45, 57, 62, 176, 188 “what” and “where” pathways see brain
Tiktaalik 33, 33–34, 34, 35, 42 words; see vocabulary
toes 45, 68–69, 71, 155–156 working memory 202, 246–247
tools, use by humans: brain mechanisms of planning writing, evolution of 275–276
200–204; comparison of ape and human tool
behaviors 199–200; handedness 173–175 X chromosome 124, 172
tools, use by primates: brain size 184–186;
comparison of ape and human tool behaviors Y chromosome 14, 16, 82, 91
199–200; cultures around 182–184; evolution of

Cognitive Evolution From Single Cells To The Human Mind

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When Cognitive Evolution first appeared, it immediately became a foundational text for all

David B. Boles is Professor Emeritus of Psychology, University of Alabama, Tuscaloosa.

ISBN: 978-0-367-68507-2 (hbk)

by Madeline Boles, age 6, published with permission

6 The mechanical and chemical senses 95

10 Praxis and handedness 163

How did life begin?

Figure 1.1 The structure of RNA and DNA.

… In a warm little pond?

Box 1.1 Cyanide and the origin of life

If not in a “warm little pond”, could life have begun…

… Around black smokers?

… In a nuclear geyser system?

Membranes and metabolism

Box 1.2 Viruses and their relationship to one-celled life

Figure 1.4 Stromatolites in Western Australia.

The workings of evolution

Descent with modification and natural selection

Box 2.1 The fossil record

The linear molecular clock

25 Old World monkeys

Kingdom: Animalia (animals)

The nonlinear molecular clock

Box 2.2 The two ages of a taxon

The tree of life

The Cambrian explosion

(caption on next page)

Figure 2.4 Section of amphioxus.

Figure 3.1 Fossil of Myllokunmingia fengjiaoa, a probable early vertebrate.

Visual system changes

Figure 3.2 A reconstruction of Tiktaalik.

Figure 3.5 Reconstruction of Westlothiana lizziae, one of the oldest amniotes.

Figure 3.7 A recent reconstruction of Archaeopteryx, a 150-million-year-old dinosaur.

Figure 3.8 Eomaia, a 125-million-year-old eutherian from China.

Box 4.1 Mammals and their parasites

The demise of nonavian dinosaurs 66 million years ago was followed by a

Table 4.1 Geological epochs immediately before and following the

Late Cretaceous 101-66 million years ago (mya)

The strepsirrhine-haplorhine divergence

Figure 4.1 Carpolestes simpsoni.

Figure 4.3 Ring-tailed lemur.

Figure 4.4 Northern greater galago.

Divergence Living examples Remainder clade Date

strepsirrhines lemurs, galagos haplorhines 68 mya

The platyrrhine-catarrhine divergence

Figure 4.5 Tarsier.

Figure 4.6 Artist’s conception of Eosimias.

New World monkeys

Figure 4.13 Aegyptopithecus skull at the University of Zurich.

Old World monkeys

Figure 4.14 Rhesus macaque.

Figure 4.15 Guinea baboon.

The ape divergences

Figure 4.16 Grey langur.

Figure 4.17 Proconsul reconstruction at the University of Zurich.

Figure 4.18 Orangutan in multibranch suspension.

Figure 4.19 White-handed gibbons.

Figure 4.20 Western gorilla.

resumed, permitting speciation (Takemoto, Kawamoto, & Furuichi, 2015). Nevertheless