How Vertebrates Left the Water

How Vertebrates Left the Water

How Vertebrates

Left the Water

Michel Laurin

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University of California Press

Berkeley and Los Angeles, California

University of California Press, Ltd.

London, England

English edition © 2010 by the Regents of the University of California

Systématique, paleontologie et biologie évolutive moderne: l’exemple de la sortie des eaux chez les vertébrés.

First published in the French language by Ellipses. © 2008 Edition Marketing S.A.

Library of Congress Cataloging-in-Publication Data

Laurin, Michel.

[Systématique, paléontologie et biologie évolutive moderne. English]

How vertebrates left the water / Michel Laurin.

p.  cm.

Includes bibliographical references and index.

ISBN 978-0-520-26647-6 (cloth : alk. paper)

1. Vertebrates—Evolution. I. Title.

QL607.5L3813    2010

596.13'8—dc22

2010027056

16   15   14   13   12   11   10

10   9   8   7   6   5   4   3   2   1

The paper used in this publication meets the minimum requirements of ANSI/NISO

Z39.48-1992 (R 1997)(Permanence of Paper).

Front cover: Paleozoic amphibians. Artist: Douglas Henderson.

Back cover: Seymouria sanjuanensis. Photographer: David Berman.

Used with permission of the Carnegie Museum of Natural History and The Museum der Natur, Gotha, Germany.

I dedicate this book to my wife, Alexandra, and my

daughter, Pénélope, who must have both felt

neglected sometimes when I spent long hours in

front of my computer working on this book and

related projects.

CONTENTS

Preface

ONE     HOW CAN WE RECONSTRUCT EVOLUTIONARY HISTORY?

Classification and Biological Nomenclature

Modern Phylogenetics

Homology and Analogy: Lungs, Swim Bladders, and Gills

Geological Time Scale and the Chronology of a Few Key Events

A Few Relevant Paleontological Localities

TWO     CONQUEST OF LAND: DATA FROM EXTANT VERTEBRATES

Are Animals Still Conquering the Land Today?

The Coelacanth, a Living Fossil?

Dipnoans: Our Closest Extant Finned Cousins

Reproduction among Tetrapods: Amphibians Are Not All Amphibious!

THREE     PALEONTOLOGICAL CONTEXT

The Conquest of Land in Various Taxa

The History of Our Ideas about the Conquest of Land by Vertebrates

The Lateral-Line Organ and the Lifestyle of Paleozoic Stegocephalians

FOUR     VERTEBRATE LIMB EVOLUTION

The Vertebrate Skeleton

Hox Genes and the Origin of Digits

Sarcopterygian Fins and the Origin of Digits

Fragmentary Fossils, Phylogeny, and the First Digits

The Gills of Acanthostega and the Original Function of the Tetrapod Limb

Bone Microanatomy and Lifestyle

FIVE     DIVERSITY OF PALEOZOIC STEGOCEPHALIANS

Temnospondyls

Embolomeres

Seymouriamorphs

Amphibians

Diadectomorphs

Amniotes

Stegocephalian Phylogeny

SIX     ADAPTATIONS TO LIFE ON LAND

Limbs and Girdles

Vertebral Centrum and Axial Skeleton

Breathing

The Skin and Water Exchange

Sensory Organs

SEVEN     SYNTHESIS AND CONCLUSION

Conquest of Land and the First Returns to the Aquatic Environment

Why Come onto Land?

Modern Paleontology and the Indiana Jones Stereotype

Glossary

Bibliography

Index

PREFACE

Life appeared in the oceans in a past so distant that it is difficult to imagine. The exact age of life on Earth is debated because the structures once considered to represent the oldest fossils (remains of ancient organisms, or traces which they left) have been reinterpreted as mineral crystallization in microscopic fractures by some paleontologists (this reinterpretation is itself debated). The first life forms were very simple and resembled extant bacteria, some of which formed stromatolites, the oldest of which are about 3 Ga (billion years) old (Fig. p.1). Stromatolites are still being formed today in some coastal regions. For at least 1.5 Ga, life remained in its native aquatic environment. Thus, for the greatest part of the history of the biosphere, life remained in water, diversified, and radiated into several ecological niches. The oceans and seas teemed with life well before the first animal ventured out of the water.

In the last few hundreds of millions of years (Ma), life has come onto dry land. This transition was very gradual; it was initiated by simple life forms, such as bacteria. Later, more complex organisms ventured onto land: lichens, simple green plants (the first of which were mosses, horsetails, and lycopods), arthropods (arachnids, insects, crustaceans, etc.), mollusks (slugs and snails), annelids (earthworms, leeches), and vertebrates. Despite their late arrival in this new environment, vertebrates will be emphasized in this book because they include humans and nearly all our domestic animals (dogs, cats, birds, cattle, sheep, pigs, horses, etc.). Thus, most readers are probably more interested in vertebrates than in any other group.

Figure p.1. Cnidarians. The first metazoans (animals with several cells) were all marine. Cnidarians are among the oldest and simplest metazoans. Reproduced from Haeckel (1904).

The conquest of dry land is a fascinating evolutionary problem because all systems and organs of our distant ancestors had been adapted to their aquatic habitat through hundreds of millions of years of evolution. This episode in the history of life on Earth is probably one of the most difficult to understand, and precisely because of this, it is no doubt one of the most interesting. The problems that our ancestors had to solve were so severe that some creationists have used them to try to cast doubt on the scientific study of biological evolution and to try to strengthen the case of their creationist explanation (this word is not entirely appropriate in this context) of biodiversity. We will see that scientists have formulated several theories that explain this fascinating history, and that one of the main challenges of modern paleontology consists of testing these theories through more or less indirect methods.

This book summarizes what we know about this history, without hiding the gaps that remain in our knowledge. It also presents the methods used by paleontologists, these detectives of life history, to reconstruct our distant past. To avoid the excessive simplifications that too often reduce this type of book to just-so stories, a few technical terms, for which there is no vernacular equivalent, must be introduced. The reader should refer to the Glossary, which includes all these technical terms. Despite the modular organization of this book, I advise reading Chapter One, How Can We Reconstruct Evolutionary History? first. A brief section on extant vertebrates illustrates the surprising amount of data that can be extracted from contemporary species, but for obvious reasons, the emphasis of this synthesis is on fossils and the evolution of the first land vertebrates. Finally, in the conclusion, the reader will discover that, contrary to the Indiana Jones stereotype, paleontologists do not necessarily spend a great proportion of their time excavating fossils in the field, and that a major part of the most fundamental discoveries results from the study of fossils first described by older generations of scientists, or from sophisticated analyses of databases that centralize data that have long been available but used to be scattered.

This book is mostly for life and earth science students who want to learn the basics of modern paleontology, systematics, and evolutionary biology, or those interested in the history of the conquest of land by vertebrates. It requires little prior knowledge in this field. Some points are covered in sufficient detail to give the reader a sense of how science works, but this book does not attempt to cover all relevant facts, because this would result in a much larger work. Those who want to know more will find the key publications in the bibliography; they can also consult the exhaustive reviews of Devonian limbed vertebrates by Clack (2002, 2006). Another recent and very technical synthesis (Hall, 2007) covers the diversity, function, and evolution of fins and limbs and presents points of view not all of which are compatible with those found in this book (see Laurin, 2007). The history of our ideas about the origin and first evolutionary radiation of limbed vertebrates was recently summarized by Coates et al. (2008). Finally, a detailed review of the hypotheses about the origin of extant amphibians was recently published (Anderson, 2008), along with a commentary presenting a different perspective (Marjanović and Laurin, 2009).

This is a translation of a book initially published in French (Laurin, 2008b). The text and bibliography were updated (several papers published in 2008 and 2009 were added), and a few references to especially important older studies were also added.

To the reader who may wonder how paleontological research can be useful, I answer simply that it enables us to know our distant history. Like archeology, paleontology is a historical science. Such research does not normally lead to patents, but it enables us to satisfy our curiosity and it has played an important role in the development of science fiction, especially since the discovery of Mesozoic dinosaurs. From Jules Verne’s Journey to the Center of the Earth through Michael Crichton’s Jurassic Park, paleontology has played a central role in popular culture. The reader will discover that reality can be as fascinating as fiction.

I thank the colleagues who helped me write this book. Joseph Segarra has given me much advice and many comments on the French edition of this book. Various colleagues (Vivian de Buffrénil and Louise Zylberberg) and students (Aurore Canoville, David Marjanović, and Laëtitia Montes) of the team Squelette des vertébrés have proofread chapters of the French edition of this book. Christopher A. Brochu, Stephen Godfrey, Michael S. Y. Lee, David Marjanović, Sean P. Modesto, and Robert R. Reisz read chapters of this English translation. Douglas Henderson allowed me to reproduce his very nice reconstructions of early stegocephalians in their habitat. My former thesis advisor, Robert R. Reisz, has played a central but indirect role in drawing my attention to Paleozoic stegocephalians and in communicating his enthusiasm for the study of this episode in vertebrate evolution. My greatest debt lays with my parents, who have always actively supported my studies, and even the fairly bold project (which I had first imagined in the 1970s) of becoming a paleontologist.

CHAPTER ONE

How Can We Reconstruct

Evolutionary History?

Our first ancestors were all aquatic. The oldest known vertebrates are about 500 Ma old, but the first potentially terrestrial vertebrates are less than 350 Ma old. For more than 150 Ma, our ancestors swam with their fins and breathed through their gills; on dry land, these structures were very inefficient. Their sensory organs worked poorly in air, if at all, and had to undergo various modifications to adapt to life on the continents. The eyes of our ancestors lacked eyelids and tear glands and could dry out rapidly; their ears did not enable them to hear most airborne sounds, such as the vocalizations of many frogs, birds, and mammals, such as the human voice. Yet all these problems were solved, and the few vertebrate species that succeeded in adapting to this new environment about 320 Ma ago diversified into the more than 25,000 extant species of land vertebrates.

To reconstruct this history, we need objective methods to use the indirect information on evolution provided by fossils or the extant biodiversity, as well as principles of nomenclature to produce classifications. These techniques and concepts are widely used in modern evolutionary biology. Thus, phylogenetics provides evolutionary trees that are the starting point of comparative or biodiversity analyses for a broad range of evolutionary problems or taxa. Biological nomenclature provides rules that enable systematists to present classifications (better called taxonomies) to summarize the evolutionary relationships between species and to sort our knowledge of the biosphere. Recent developments in phylogenetics and, to a lesser extent, in biological nomenclature have given new life to paleontology and evolutionary biology. Until approximately the 1970s, paleontologists reconstructed evolutionary trees by hand, using criteria that they did not always explain. Since then, the advent of cladistics, soon followed by software that enabled systematists to tap into the tremendous processing power of computers, introduced more objectivity into phylogenetics because the data used to produce the trees are generally published. This triggered a proliferation of phylogenetic studies and led to a re-examination of many long-held hypotheses on the phylogeny of life. As a result, we now have a much better resolved tree of life than a few decades ago, even though much of this tree will probably change as a result of future investigations. These methods are presented in a simplified manner in this chapter, and the bibliography provides an introduction to the most relevant papers where more technical information can be found.

CLASSIFICATION AND BIOLOGICAL

NOMENCLATURE

Rank-Based Nomenclature

A form of classification is essential to sort information, whatever its nature. Man has classified animals since antiquity, as attested in the Bible (ESV, 2001), in which we can read: So out of the ground the Lord God formed every beast of the field and every bird of the heavens and brought them to the man to see what he would call them. And whatever the man called every living creature, that was its name. (Genesis, 2:19). Since Aristotle (384–322 BCE), many authors have proposed classifications of living beings. The subdiscipline of biology that consists of naming, defining, and delimiting the groups of living organisms (the taxa) is called taxonomy, like the product of this activity (the taxonomies). Thus, taxonomy harks back to antiquity (under a form substantially different from today’s), but, initially, only vernacular names were used. These were part of the standard vocabulary of a language, in contrast to formal names that are often known only by scientists.

The drawback of vernacular names is that their meaning can vary in space and time (this is typical of most words in any language), and there are often no exact synonyms among languages. Thus, the word fish once included whales (until the 19th century), although they are now excluded because we now know that whales are mammals that have returned to the seas. In English, this word has also included, at least in its broadest sense, aquatic animals that are no longer considered fishes, such as echinoderms (e.g., starfish), arthropods (e.g., crayfish), mollusks (e.g., cuttlefish), or even cnidarians (e.g., jellyfish); but this is not true of many other European languages, such as French, in which the equivalent word poisson has long had a narrower sense restricted to aquatic vertebrates. These two words (fish and poisson), often considered synonyms, have thus not always referred to the same groups of animals.

Vernacular words are not ideally suited to scientific use because of their variability in space and time, and because of the imperfect synonymy between names used in various languages (Minelli et al., 2005). Thus, scientists began to develop, as early as the 18th century, precise taxonomies based on names that would ideally have the