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Morphology and behaviour: functional links in development and evolution

Introduction

Article in Philosophical Transactions B · July 2011

DOI: 10.1098/rstb.2011.0035 · Source: PubMed

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 Phil. Trans. R. Soc. B (2011) 366, 2056–2068
doi:10.1098/rstb.2011.0035

Introduction

Morphology and behaviour: functional links

in development and evolution
Rinaldo C. Bertossa*
Centre for Behaviour and Neurosciences & Centre for Ecological and Evolutionary Studies, University of
Groningen, PO Box 11103, 9700 Groningen, The Netherlands
Development and evolution of animal behaviour and morphology are frequently addressed indepen-
dently, as reflected in the dichotomy of disciplines dedicated to their study distinguishing object of
study (morphology versus behaviour) and perspective (ultimate versus proximate). Although traits
are known to develop and evolve semi-independently, they are matched together in development
and evolution to produce a unique functional phenotype. Here I highlight similarities shared by
both traits, such as the decisive role played by the environment for their ontogeny. Considering
the widespread developmental and functional entanglement between both traits, many cases of
adaptive evolution are better understood when proximate and ultimate explanations are integrated.
A field integrating these perspectives is evolutionary developmental biology (evo-devo), which
studies the developmental basis of phenotypic diversity. Ultimate aspects in evo-devo studies—
which have mostly focused on morphological traits—could become more apparent when behaviour,
‘the integrator of form and function’, is integrated into the same framework of analysis. Integrating a
trait such as behaviour at a different level in the biological hierarchy will help to better understand
not only how behavioural diversity is produced, but also how levels are connected to produce func-
tional phenotypes and how these evolve. A possible framework to accommodate and compare
form and function at different levels of the biological hierarchy is outlined. At the end, some
methodological issues are discussed.
Keywords: evo-devo; evolutionary developmental biology; evolution of behaviour; emergence;
levels of analysis; biological hierarchy

1. INTRODUCTION to name a glossy subject, has begun to realize the impor-

Behaviour has been studied for decades from both tance of evolution, not only in its large praxis [6,7] but
proximate (i.e. ontogenetic mechanisms and causes of also for addressing specific and burning issues such as
actual behaviour) as well as ultimate perspectives (i.e. cancer [8].
survival value and evolution) [1]. Is there a need for a A discipline that is successfully integrating proximate
new perspective? In recent years, fostered by unprece- with ultimate aspects of phenotype is ‘evolutionary
dented technical developments, we have noticed a new developmental biology’, or evo-devo in short. Evo-
way to address (classic) questions that makes use of a devo, as defined by one of its early exponents, is ‘the
more integrative approach and focuses on the system study of how developmental processes evolve to produce
in addition to its component parts (e.g. [2,3]). On the new patterns of development, new developmental gene
other hand, different disciplines join forces to answer regulation, new morphologies, new life histories and
common questions. A clear trend is the integration of new behavioural capabilities’ [9]. Evo-devo has recorded
proximate and ultimate perspectives for a comprehen- many important achievements [10] and has now a diver-
sive understanding of phenotypes. But why combine sified research programme that ranges from comparative
development with evolution? A quick, off-the-shelf embryology and morphology, developmental genetics to
answer is: because ‘nothing in biology makes sense theoretical approaches [11].
except in the light of evolution’ [4]. The fact is that, Although evo-devo has successfully succeeded in
here, this quotation is appropriate. In fact, explaining identifying developmental mechanisms underlying
phenotype and its diversity ‘is fundamentally a problem phenotype diversity (e.g. [12,13]), a more evident inte-
of explaining the evolution of phenotype development’ gration of proximate and ultimate explanations seems to
[5]. This goes beyond evolutionary biology. Medicine, be required [14,15]. The objective could be not less
than a ‘mechanistic theory’ for explaining phenotype
development and evolution [16]. Since behaviour, con-
*[email protected] sidered frequently as ‘integrator’ of form and function
One contribution of 10 to a Theme Issue ‘Evolutionary [16], plays an important role in adaptive evolution, it
developmental biology (evo-devo) and behaviour’. would be ‘simplistic, and indeed potentially misleading,
2056 This journal is q 2011 The Royal Society
 Introduction. Morphology and behaviour R. C. Bertossa 2057

to consider the evolution of form without taking into functional phenotype while analysing individual traits
account its interactions with behaviour in the arena of may help to better understand aspects of their develop-
selection’ [10]. Although notable efforts to consider ment and evolution, as I discuss here.
development and evolution of organisms within
their natural context—and highlight so the role of
(a) Developmental aspects
behaviour—are being made (e.g. [17,18]), evo-devo
(i) When does development of behaviour begin?
studies have mostly focused on morphological
While a distinction may be made between a morpho-
aspects of the phenotype, leaving behaviour largely
logical and a behavioural trait, a clear separation
unaddressed [19].
between development of morphology and behaviour
The present issue is a first, more direct attempt to
does not exist. When does behaviour, and so its
address behaviour within an evo-devo framework. The
development, begin during the lifetime of an animal?
first obvious benefit we can expect is to understand
Development of behaviour may be considered as
more about the developmental mechanisms underlying
beginning when the organism interacts with the environ-
behaviour diversity. But there is another, complemen-
ment. But what is the environment? Is this the ambience
tary interest peculiar to addressing traits at different
external to the developing organism? In many classical
levels of biological organization, such are morphology
examples, behavioural development starts already
and behaviour. Although organisms develop and
before a mature behaviour is ‘used’ to interact with the
evolve as functional unitary entities, they are composed
external world [21]. For instance, highly specific respon-
of a hierarchy of levels (i.e. proteins, cells, organs and
siveness to the mallard maternal call at the species-typical
so on) [20]. To achieve the fitness of the whole, the indi-
repetition rate develops in the Peking duck embryo in
vidual parts are matched. To understand how the levels
advance of auditory experience with its own or sib voca-
are matched to each other and how variation at the
lizations [22]. Similarly, correct wiring of the visual
genetic level translates into a functional phenotype (up
system in higher mammals occurs in utero long before
to behaviour), it is crucial to understand the kind of
vision, when waves of spontaneous neuronal activity
relationships that connect levels. A hypothesis could
are generated by ganglion cells in the retina, even before
be that different levels of biological organization may
photoreceptors are present, and propagated across cen-
share principles of development and evolution and
tral synapses to target neurons in the lateral geniculate
that, by looking at one level, one may discover principles
nucleus [23]. In these cases, development of behaviour
that are relevant for others. Conversely, principles may
starts during embryogenesis. Basically, neuronal circuits
be level-specific and focusing on only one level or even
underlying behaviour develop long before the behaviour
a priori assuming that principles obtained by studying
they support, and the stimulation of many of them is
one level can be applied tout court to other levels may
crucial for their development [24].
be misleading. It is hence important to extend the evo-
Thus, the distinction between the internal and the
devo paradigm to other levels of the biological hierarchy
external environment in order to define when develop-
and include the whole functional phenotype [10].
ment of behaviour begins is problematic. Further, if
In this introductory article, I am mainly concerned
influences internal to the developing organism can be
with showing that morphology and behaviour share
considered part of ‘behaviour development’, which of
many aspects, beginning with the importance that the
these should be viewed as behaviour development and
environment plays for their development. Behaviour and
which not? The development of many neuronal circuits
morphology constitute in fact different qualities of the
underlying behaviour does not require action potentials
same unique phenotype, tightly linked in development
and synaptic transmission but is regulated by molecular
and evolution. Since these qualities appear to be present
cues as found on cell surfaces or diffusing in tissues, the
at each level of the biological hierarchy, a unique frame-
same class of signals that regulate morphological develop-
work of analysis encompassing levels seems already
ment [25]. How should the reaction of a neuron (growth;
possible. Based on that assumption, I provide an example
changing neuronal activity) later involved in behaviour to
of comparison across levels and discuss some impli-
an impinging stimulus be categorized? Morphological or
cations. I conclude with some critical considerations on
behavioural development? In an extreme view, behaviour
methods used for discovering the genetic basis underlying
can be simply considered as a series of neuronal impulses
behavioural diversity. At the end of the article, summaries
within a specified neuronal circuit. In this case, develop-
of the contributions presented in this issue can be found.
ment of behaviour would start when the first neuron is
formed. From the perspective of a developing neuronal
circuit and neuronal impulses (and hence for behaviour),
2. DIFFERENT TRAITS, ONE PHENOTYPE
it does not matter whether a stimulus comes from outside
In order to facilitate analyses, the phenotype is often
or inside the developing organism or whether it has a
fragmented in distinct traits and every trait analysed
chemical or neuronal origin: it will cause a change in
separately. This is reflected also in the disciplines dedi-
developmental events. Thus, development of behaviour
cated to the study of the different traits, such as
and morphology merges at a certain point into each
developmental biology (i.e. morphology) and ethology
other, but where?
(behaviour), as well as their perspectives, such as prox-
imate (e.g. developmental genetics) and ultimate (e.g.
behavioural ecology). However, although the indepen- (ii) Development of both morphology and behaviour
dence of traits in development and evolution is a is sensitive to environmental influences
known phenomenon [5], organisms develop and Changing perspective on what to consider ‘envi-
evolve as one entity. Keeping an eye on the whole ronment’ helps us to recognize more similarities
Phil. Trans. R. Soc. B (2011)
2058 R. C. Bertossa Introduction. Morphology and behaviour

shared by morphology and behaviour. Plasticity is system in mice, for instance, requires sensory feedback
‘the ability of an organism to react to an internal or from muscle contractions to adjust correct synaptic
external environmental input with a change in form, organization [30]. An extreme example illustrating
state, movement, or rate of activity’ [5]. Behaviour this mutual influence is provided by the so-called
is commonly viewed as ‘the’ plastic phenotype, ‘one two-legged goat and discussed by West-Eberhard [5].
organismal property that displays high degrees of The goat, born without forelegs, adopted a semi-
phenotypic plasticity’ [16]. Certainly, behaviour is upright posture and bipedal locomotion from the
‘highly, and reversibly, combinatorial and recombina- time of its birth. This behaviour caused morphological
torial during a single life time’ [5], but this is a changes in bones, pelvic skeleton and musculature
quality of a trait as it appears in a specific moment. and thoracic skeleton not found in normal goats of
And yet, also its development is considered as being the same age. Besides demonstrating the interplay
particularly plastic, in which the continuous inter- between morphology and behaviour in development,
action with the environment is an intrinsic property. this example reveals something else: development is
Experience and learning are concepts commonly contingent and accommodating. That is, if there is a
associated with that. Morphological development, in ‘developmental programme’, this is highly sensitive
contrast, is mostly believed to be less influenced by to feedbacks from the environment. If these change,
environmental perturbations. But which environment then developmental events can, to a certain degree,
are we talking about? adapt. Changes in the environment can have a genetic
If we shift the focus away from the whole organism origin (e.g. altered expression of a transcription factor
and define ‘environment’ as everything different during limb development) but also a non-genetic basis
from the genome [5], we realize that the develop- (e.g. paralysis of forelimbs owing, for example, to
ment of morphology is highly plastic and does not polio). It is clear that there was no ‘programme’ telling
require fewer interactions with the environment than a priori that bones and muscles should have developed
behaviour does. Morphological development relies on in a certain way if some components had changed.
continuous interactions between developing parts of There were no genes telling the limbs to develop
the body. For instance, shear stress produced during differently or telling the animal to behave differently.
flow is necessary for the correct development of The ability to adapt to changing developmental
haematopoietic cells [26]. A classical example in mor- conditions—regardless of the cause of variation, whether
phogenesis is neural induction, when the mesoderm genetic or environmental—is known as phenotypic
contacts and induces the overlying ectoderm to accommodation [5]. But a changing environment, we
develop into neural tissue. Manipulations of develop- have seen, is a constant of all development, not only
mental events reveal how crucial the environment is of a pathological state. Indeed, many aspects of pheno-
for a ‘normal’ morphological development: if a small type development simply emerge from interactions in
piece of tissue from around the dorsal rim of the blasto- time and space of underlying component parts and do
pore of a developing amphibian embryo is transplanted not probably map one-to-one onto a genetic ‘pro-
to the ventral side of another embryo, the host responds gramme’. For instance, if shear stress is a key player
by forming an additional embryonic axis containing a vir- for the development of haematopoietic cells, how is
tually complete central nervous system [27]. Interactions this information encoded in the genome? Is there a
among developing tissues can certainly be viewed as a gene or genetic programme ‘dedicated’ to ‘shear
process of ‘experience and learning’, not less than what stress’? For this reason, it has been argued that organ-
is known for development of behaviour. Not surprisingly, isms are not reducible to the component parts [31,32]
sensitive periods—phases in development during which a and several authors [5,33–35] warn against seeing a
specific trait of an organism can be permanently altered strictly defined ‘programme’ in the genome and con-
by a particular experience or treatment, preceded and fol- sidering genes as the sole source of developmental
lowed by a period of lower sensitivity to the same information.
treatment—are readily described in behavioural [28] as This realization has been made earlier in behavioural
well as morphological development [29]. sciences. Probabilistic epigenesis for instance ‘empha-
When stressing the role of the environment in sizes the reciprocity of influences within and between
development and evolution [16], it is important to levels of an organism’s developmental manifold’ (like
realize that the environment internal to a developing genetic activity, neural activity as well as influences of
organism plays a role as important as the environ- the environment external to the developing organism)
ment external to it. But basically, external/internal are ‘and the ubiquity of gene – environment interaction
relative concepts. What is external to the cell is internal in the realization of all phenotypes’ [36,37]. Similarly,
to a tissue, which is internal to an organ and the organ- in neuroconstructivism, ‘cognitive development is
ism. Even stimuli impinging on an organism may still be explained as emerging from the experience-dependent
considered internal to a social group, a colony and so development of neural structures supporting mental
on. The best focus for an integral evo-devo is simply representations’ [38].
the whole functional phenotype, which may be defined, Attempts to include the environment into a theory
according to one definition, as ‘all traits of an organism of development and evolution are being made in
other than its genome’ [5]. ‘developmental systems theory’ (DST), which—not
surprisingly—is rooted primarily in developmental
(iii) Genes and environment and behavioural psychology. For DST ‘developmental
Morphology and behaviour influence each other’s information resides neither in the genes nor in the
development. Development of the withdrawal reflex environment, but rather emerges from the interactions
Phil. Trans. R. Soc. B (2011)
 Introduction. Morphology and behaviour R. C. Bertossa 2059

of disparate, dispersed developmental resources’ [39]. phenotype. Behavioural ecology has thrived on verify-
While genes play clearly an important role in develop- ing theoretical predictions in natural populations [48]:
ment, they do not seem to be alone. But who plays which is the best behaviour to survive in a particular
which role is still debated [40]. An important question ecological context? But where does behavioural diver-
is thus understanding which the other developmen- sity in developmental terms come from? ‘How comes
tal resources are, the role they play, and whether this diversity to be there in evolutionary terms?’ [5].
and how they could be integrated into the evo-devo As exemplified by the two-legged goat, new behaviour
framework of analysis. may be the result of phenotypic accommodation or of
ancestral inheritance instead of selective pressure alone
[49,50]. Moreover, the past evolutionary history con-
(b) Evolutionary considerations
strains future evolutionary trajectories [51,52]: under
(i) Reciprocal influences in evolution
the same selection pressure, different genomes will
Evolutionary studies have preferred to focus either on
respond in different ways, whereas similar traits can be
morphology or on behaviour. However, if the pheno-
the result of different developmental paths [53,54].
type develops as one entity, reciprocal influences in
Thus, functional considerations may be used to predict
evolution are expected, as described in several studies
successful behavioural strategies such as particular cog-
on adaptive evolution.
nitive abilities [55], but probably not to predict their
McPeek [41] compared Damselfly larvae of species
genetic and developmental basis [56–58]. Behaviour
inhabiting lakes in which predation was exerted by
observed in an animal is the result of the interplay
fishes and of species from fish-less lakes, in which
between genetic and developmental constraints as well
dragonflies were the main predators. The latter are mor-
as selection pressures [59].
phologically very similar to one another and differ greatly
A topical example to illustrate the above are behav-
from fish-lake species. They are large and are active
ioural syndromes, ‘a suite of correlated behaviours
swimmers. All larvae of species from lakes with fishes
reflecting between-individual consistency in behaviour
move very slowly and infrequently but species are
across multiple situations’ [60]. Their existence
morphologically very diverse. Since species in fish-less
appears in conflict with the expectation that organisms
lakes are more closely related to species in lakes with
are adapted to every situation in an optimal fashion.
fishes, McPeek concluded that, following habitat shifts,
Without knowing the genetic and developmental
selection pressures exerted by dragonfly predation
basis of behaviour, it is not possible to fully explain
apparently favoured swimming as an escape tactic,
why behavioural syndromes are present in some
which mediated selection pressures onto morphologies
species but not in others, or why behavioural syn-
used in swimming to increase swimming performance.
dromes display in some species correlations across
Similar considerations may apply in other cases. Adap-
domains (e.g. aggression in feeding as well as mating
tive differences in the jaw morphology in cichlid fishes
domain) whereas in others they show domain-specific
are related to their feeding habits [42], and the same
correlations (e.g. in the mating domain, correlation
seems true for variations in beak morphology in
between aggression towards females and males; no
Darwin finches [43]. In more extreme cases, such as
correlation between aggression in the mating versus
the evolution of secondary male sexual ornaments,
feeding domain) [61].
which in some species are driven by female choice
Another conundrum is explaining the adaptive evol-
[44], the function of morphological structures can only
ution of similar (or homologous) behaviours in
be understood in conjunction with behaviour. These
different taxa (figure 1). Not only are common beha-
are just a few examples but the ‘potential complexity of
viours like aggression, sex, or learning and memory
morphological and behavioural interactions in the evol-
present across taxa [63], but also more specific ones,
ution of new adaptive types’ could be ‘much greater
such as tool use [64] or web-spinning [65]. A key devel-
than previously considered’ [45].
opmental question is: can similar behaviours in different
All elements of the phenotype influence, directly (e.g.
taxa rest upon completely different neuronal and/or
neurons) or indirectly (e.g. muscle size), patterns of
genetic mechanisms or do similar behaviours (indepen-
behavioural adaptation. Katz [46] argues that the func-
dently of the taxon) rely (or even have to rely) on
tional organization of the nervous system constrains
conserved neuronal and/or genetic mechanisms
but also promotes the evolvability of behaviour, and
(figure 1)? Answering this question correctly also
Chiel & Beer [47] remind that ‘adaptive behaviour also
depends on clarifying what ‘homologous’ traits are.
depends on interactions among the nervous system,
Homology in biology refers to an historical continuity
body and environment: sensory preprocessing and
of traits. As aptly formulated by Wagner [66], ‘intui-
motor post-processing filter inputs to and outputs from
tively, one would expect that the historical continuity
the nervous system; coevolution and co-development
of morphological characters is underpinned by the con-
of nervous system and periphery create matching and
tinuity of the genes that govern the development of these
complementarity between them; body structure creates
characters. However, things are not that simple: one of
constraints and opportunities for neural control; and
the most important results of the past 15 years of mol-
continuous feedback between nervous system, body
ecular developmental genetics is the realization that
and environment are essential for normal behaviour’.
homologous characters can have different genetic and
developmental bases’ [53,54,67]. These findings have
(ii) Integration of proximate and ultimate explanations occasionally caused misunderstandings as to the correct
Purely functional considerations of behaviour seem interpretation of homologous characters [68–70] and
sometimes to forget the historical dimension of the new ways to define them are being continuously
Phil. Trans. R. Soc. B (2011)
2060 R. C. Bertossa Introduction. Morphology and behaviour

genetic neuronal behaviours and in analogy with a morphological trait, the form of a
mechanisms mechanisms particular species-specific behavioural pattern (e.g. the
courtship displays) remains within certain limits (i.e. is
A A repeatable) and can be recognized as such despite some
1 A
B B intra- and inter-individual variation in members of the
same species. Additionally, this characteristic allows a par-
ticular behaviour to achieve a determined function (i.e.
A grooming behaviour, or a communication display). Fre-
2 A A
B quently, a specific motoric pattern with specific parts of
the body produces a reaction but not when the same
motoric pattern is produced with other parts of the
3 A A A
body (if possible at all) or if another motoric pattern is
produced using the same body parts. For instance, a
A hand movement in a certain fashion signals ‘hello!’
4 A A Another movement with the same hand may signify com-
B
pletely opposite intentions. This specificity is more
Figure 1. Evolution of ‘homologous’ behaviours. The evol-
evident in elementary behaviours involving motoric pat-
ution of similar behaviours across taxa, such as sex or terns such as feeding, swallowing, excreting (urinating
aggression, represents a key developmental and evolutionary and defecating), displacing in space (walking, flying),
phenomenon for understanding genetic and developmental yawning, vomiting, grooming and so on. But also more
paths through which specific behaviours can be realized. complex behaviours, such as aggression, sex, fear, to
Here, the question is whether similar behaviours can have even more elaborate functions commonly defined under
a different neuronal basis (1), whether particular behaviours the term ‘cognition’, such as decision making, may still
can only rest upon conserved neuronal (2) and genetic be characterized by having a determined ‘form’. As
mechanisms (3) or whether—as in the construction of func- known for morphological traits, motoric patterns in a
tionally similar morphological structures [62]—similar species are so constant that they can be used to classify
behaviours can have the same genetic but different neuronal
species and build phylogenies (e.g. [76,77]). The idea of
(i.e. developmental) basis (4).
form in behaviour is not new. Lorenz, for instance,
when referring to ‘Instinkthandlungen’ (instinctive acts),
insisted on viewing and studying species-specific
discussed [66,71–73]. The same kind of difficulties are behaviours as organs [78].
expected when discussing homology in behavioural
traits and, especially, their underlying genetic and
developmental bases [63]. (ii) The behaviour of form and the link to function
If the above discussion reminds us of the importance Up to here, behaviour has been considered from its etho-
to correctly [74] integrate proximate and ultimate aspects logical perspective (i.e. as ‘the behaviour of an animal’).
for an accurate understanding of behaviour [75], the But behaviour has, of course, a broader definition, as
latter example raises another, related problem: how are found for example in Wikipedia: ‘the actions or reactions
the levels in the biological hierarchy connected? of an object or organism, usually in relation to the
environment’. Behaviour so defined is not restricted to
any specific level of the biological hierarchy. Protozoa,
3. TOWARDS FORMULATING A FRAMEWORK OF for instance, display complex actions and reactions,
ANALYSIS ACROSS LEVELS OF ORGANIZATION from escaping from a threat, mating and replicating to
(a) Broadening the perspective moving towards a food source and feeding [79]. These
Upto here, I have tried to highlight the importance movements are not coordinated by a nervous system but
of keeping an eye on the whole phenotype while are nevertheless classified as animal ‘behaviour’. Basically,
studying individual traits. This helps us to recognize morphological structures at every level of the hierarchy
qualities shared by morphology and behaviour (e.g. are regularly engaged in behaviour: organs, cells and
the importance of the environment) and recipro- enzymes ‘act or react’. This ‘acting or reacting’ is strictly
cal influences in development and evolution. Here associated with function, meant here as the way in
I change perspective. I use broader definitions of which a morphological trait operates to achieve function.
‘form’ and ‘behaviour’ to develop a possible frame- The heart behaves in a defined way in order to function as
work to describe and compare traits at different a pump. Enzymes ‘behave’ (i.e. function) in a very specific
levels of the biological hierarchy. way in order to operate (e.g. catalyze reactions).
A second element in the definition is that behaviour
(i) The form of behaviour may or may not involve movement. Even structures
One apparent quality of morphology is to have a defined that appear static may owe their form to passive behav-
structure, a form. As can be found in any English diction- iour, like for instance the structure of a bone, which is
ary, form is defined as ‘the spatial arrangement of meant to maximize resilience when involved in a
something as distinct from its substance’. In that respect, specific motoric behaviour, or colour patterns on the
also behaviour has, like morphology, a form. Different exoskeleton of an insect, meant to provoke a specific
from morphology, behaviour may be viewed as a dynamic behaviour, like sexual attraction in a potential partner
(i.e. involving movement) ‘spatial arrangement of ’ e.g. or warning to competitors or other insects, or even to
body limbs, but this is nevertheless ‘form’. In this sense avoid being seen by predators.
Phil. Trans. R. Soc. B (2011)
 Introduction. Morphology and behaviour R. C. Bertossa 2061

Generally, morphological structures have a deter- (b)

mined form in view of a specific way of operating.
The way in which they operate, involving or not move- 3
ment, because it is an ‘action or reaction’, can be
considered ‘behaviour’. Put differently, the mean of
functioning (the behaviour) of a morphological struc-
2
ture reveals its (form and) function. This is why
behaviour is frequently seen as an integrator of func-
tion [16]. This is not to say that morphology does
not have function on its own, but a more correct 1
view is that function is achieved through morphology
(i.e. structure) behaving (or used ) in a specific way.

?
(iii) A framework for comparing levels of organization
Considering the similarities between morphology and (a)
behaviour highlighted above and, especially, the form
characterizing morphology as well as behavioural dis-
plays, a unique evo-devo programme may now be 2
more within reach. A common programme would for
3
instance try to understand developmental mechanisms
underlying ‘form’ at each level of the biological hierar-
chy and how these levels relate to each other. In order
1
to integrate proximate and ultimate perspectives, the
‘mechanistic theory’ for evo-devo envisioned by
Laubichler [16] should hence also integrate levels of
biological organization. With respect to ‘mechanistic
explanations’, evo-devo has been mainly considering Figure 2. Organization of levels in the biological hierarchy.
gene regulatory networks acting in development and The organization of elements at each level may be similar
changing through evolution (e.g. [80]). Yet, we have across the biological hierarchy. Because elements or parts
seen above that many features of the phenotype have (indicated by the numbers) behave or interact (indicated
emergent properties that would not map necessarily by arrows connecting the parts) in a specific way, they
one-to-one with the genotype. To the reductionistic acquire (in the case of dynamic interactions between the
criticism Hamilton replies ‘by noticing that mechanistic parts) or have (in the case of static interactions) a form
explanations are reductionistic’—in the sense that a with a defined function. (a) A level may be a protein, com-
posed of amino acids having a specific spatial organization
‘mechanistic explanation works by decomposing systems
or, (b) in a behavioural display with an arm, a determined
(. . .) into their component parts and operations’—‘but coordination in time and space of parts of the arm (hand,
they need not lead to gene-centrism’. In particular, forearm). A key question is understanding how the levels
reductionistic explanations ‘need not lead anyone to are connected (vertical double arrow with question mark).
ignore the overall system in favour of the actions of one
“fundamental” part of it [81]. That is, the properties of
a system depend as much on the component parts as which parts at a certain level of the biological hierarchy
on their organization. are organized and function. As soon as this organiz-
By reuniting the qualities of form and behaviour ation changes in time or space, development begins.
outlined above, one may recognize that ‘behaviour’— A ‘mechanistic theory’ for development and evol-
in its broader definition—is in fact the way in which ution would thus have to understand (i) which are
parts composing a specific level of the hierarchy func- the parts composing each level in the biological hierar-
tion, their organization. The parts so organized (i.e. chy, (ii) how these parts are organized in order to
behaving in a certain way) acquire and have a specific produce each level, (iii) how the levels are connected,
‘form’ and so a function. This perspective applies to and (iv) how the organization in levels evolves and
any level of the biological hierarchy (figure 2). Parts affects evolutionary trajectories in order to produce
at the ‘behavioural level’ may be body parts that, orga- phenotypic diversity.
nized (i.e. moving, behaving) in a specific way, achieve
a certain function; parts at a lower level may be amino
acids in a protein that, organized in a determined way (b) Evo-devo on behaviour: comparing levels
(i.e. having a specific three-dimensional structure) If developmental mechanisms are similarly organized
achieve a specific function. through the levels of the biological hierarchy, then con-
In this way, some of the difficulties encountered served principles may be expected across them. An
above, as for example establishing when, during devel- approach to understand this is applying the available
opment, to consider the beginning of behaviour evo-devo framework to what we already know about
development, would disappear. Because biological development and evolution of behaviour (see e.g.
systems are inherently functional, they are always com- [82]). Here, I briefly illustrate an example of how
posed of behaviour and form at the same time. Form this approach could look like and generate new specific
and behaviour describe together the specific way in questions that can be experimentally addressed.
Phil. Trans. R. Soc. B (2011)
2062 R. C. Bertossa Introduction. Morphology and behaviour

(i) The conservation of developmental elements to behaviour are probably involved in other, non-
across species behavioural functions [105]. The genes needed for the
An ongoing discovery in evo-devo studies is that many construction of the central nervous system (e.g. Hox,
genes and gene regulatory networks underlying mor- Otx, Pax, Wnt), for instance, are used for the construc-
phology are evolutionarily conserved and inform the tion of other organs as well [106]. This applies also for
evolutionary process [83]. Some are used for similar many genes (e.g. Pax6) involved in the development of
tasks in distant taxa, such as genetic cascades underlying central pattern generators (CPGs), neuronal circuits
eye [62] or heart [84] formation, or for the specifica- underlying many rhythmic behaviours like breathing
tion of proximal–distal limb patterning [85]. Others are and walking [107]. This could suggest that also diversity
deployed multiple times during development for the in behaviour may be produced mainly through changes
construction of completely different structures [86,87]. in the use rather than the coding sequence of genes, a
Is there conservation in the elements (genes, neurons) hypothesis supported already by few data. For example,
underlying behaviour? Some behaviours, like aggres- an important species-specific difference in affiliative be-
sion [88] or learning [89], seem to rely on molecular haviour in voles is caused by changes in the regulatory
mechanisms that are conserved between vertebrates and region of the vasopressin V1a receptor [108]. The fact
invertebrates [63] (see also [63] for a broader discussion). that in humans, retained non-coding sequences under-
This might be explained by the fact that a centralized ner- went accelerated evolution compared with other
vous system was already present in the common ancestor primates [109], and genes specifically expressed in the
of bilateria, as supported by genetic and developmental brain display a lower degree of amino acid divergence
data [90,91]. These data suggest that even more molecular than other genes [110], lent further support for such a
mechanisms underlying ‘homologous’ behaviours could mechanism. Finally, since FoxP2 is expressed in vocal
be shared by vertebrates and invertebrates. It may hence learner and non-vocal learner species, its involvement
not be surprising to find conservation within more related in vocal learning has also been attributed to differences
groups. FoxP2, for instance, even though it is also in expression [92].
expressed in non-vocal learner species, is necessary for With regard to neuronal mechanisms, since homolo-
the elaboration of sensory-motor information underlying gous neurons and neuronal circuits can be found in
vocalization from crocodiles to humans [92,93]. species that appear and act very differently, it has been
Conservation seems also to be widespread in the suggested that functional differences could arise by re-
neuronal mechanisms underlying behaviour. Neuronal specification of common circuits [19,96]. Different
structures responsible for acquisition and processing of authors have observed that rather subtle changes in
odorant and taste information display a striking degree the nervous system (e.g. change in neuromodulation)
of similarity between invertebrates and vertebrates can cause important changes in behaviour [56,96].
[59,94]. Since specific neuronal circuits can support For instance, the evolution of language in humans
different behaviours [95], conservation across taxa entailed modifications of pre-existing neuronal cir-
may not be surprising and could also explain the cuits [111] and the switch between aggression and
observation that entire circuits may be retained even courtship in Drosophila relies on the neuromodula-
across taxa that display different behaviours [96]. tory action of octopamine on male-specific neuronal
Even if limited, these data suggest that conservation circuits [112].
might not be specific to a level of the biological hierar- The first impression when considering these data is
chy (e.g. genes, proteins) but might be common also at that both at the genetic as well as the neuronal level the
other levels (e.g. neuronal circuits). Still, many ques- way for producing phenotypic diversity may be similar.
tions remain open. If elements are conserved, how That is, changes in the use (rather than the nature) of
is context-specificity during development realized? conserved elements at one phenotypic level (genes,
That is, how are conserved elements used to produce neuronal circuits) seem responsible for changes at
different developmental outcomes? Do conserved gene higher levels (morphology, behaviour). The data pre-
regulatory networks underlie particular behaviours as sented above are certainly not enough to make a
they do for particular morphological structures [83]? conclusive assessment, but the idea may still serve as
If elements (i.e. proteins, neuronal circuits) are a working hypothesis. Basic questions related to this
conserved, how is behaviour diversity produced? are: How do changes at the higher levels needed for
producing new behaviour correlate with changes at
the genetic level? Is it all about ‘teaching old genes
(ii) Developmental mechanisms underlying phenotypic (or neuronal circuits) new ‘tricks’’—to use an
novelty expression familiar to evo-devo practitioners [113]—
The fact that many proteins and protein cascades are or are other changes (i.e. the coding sequence of
conserved across taxa but are deployed for the construc- genes) also or even more important for producing
tion of different morphologies suggested that their new behaviour? Are the genetic and developmental
differential use (rather than their composition) could changes responsible for behaviour variation within
lie at the basis of the observed diversity. Since differential a species the same as those causing behaviour
gene use is obtained through changes in regulatory differences between species?
regions, this came to be considered by some as a major These few considerations already raise excitement:
mechanism behind the evolution of phenotypic novelty the conservation of principles governing development
[97,98]. Although still debated [99,100], this conclusion and evolution of phenotypes across levels of phenoty-
is supported by studies on the evolution of morphological pic complexity (i.e. morphology, behaviour) could be
and physiological traits [101–104]. Genes contributing more than a hypothesis.
Phil. Trans. R. Soc. B (2011)
 Introduction. Morphology and behaviour R. C. Bertossa 2063

4. THE SEARCH FOR GENETIC CHANGES behavioural mutants in high-throughput format

UNDERLYING BEHAVIOURAL DIVERSITY: [120,121], or microarrays and next-generation sequen-
SOME CONSIDERATIONS cing methods to spot changes in gene expression as a
(a) The limits of comparative genomics consequence of the induced mutation (see below).
How to find changes in the genome that are relevant However, understanding the primary function of a
for behavioural diversity? Comparisons between the wild-type allele by looking at the effects of its mutated
genomes of distinct species may reveal associations version could be misleading. In fact, if phenotypic
between new genes and novel phenotypes [114]. In gen- accommodation is extensive, the mutant phenotype
eral, however, as already known for new morphological we observe would be caused primarily by the reaction
structures, new behaviours are probably the product of of the developing system to the mutation, which has
conserved genes rather than new, species-specific ones. less to do with the primary function of the gene. For
For instance, the development of CPGs relies on genes instance, if the two-legged goat phenotype was
involved in the development of many other structures caused by a mutation, what is the primary function
[107]. For the same reason, it will be difficult to infer of the mutated gene? Causing the goat to walk nor-
function from the evolutionary conservation of the mally? Or should we not better say that we have
DNA sequence [115], both regulatory and coding, discovered the gene (i.e. the mutant allele) responsible
unless the compared species are closely related and for bipedal posture?
the involvement of some genes in behaviour is known Heritable behavioural variation in a population can be
at least in one species. In the case of new morphology, screened directly or used to select lines that behave differ-
relevant genes can be inferred from their expression in ently. Differences in behaviour can then be correlated
the new structure they build (e.g. [43]). As to behaviour, with genetic changes through microarrays [118], QTL
it will be difficult to associate genes with a particular be- analyses [122] or, nowadays, next-generation sequencing
haviour without knowing which specific neuronal methods [123]. Although selection is applied on behav-
elements the behaviour needs, which is rarely the case. ioural differences observed within and not between
Additionally, the fact that the same neuronal structures species, selection experiments can identify genes associ-
can support many behaviours [95] renders the analysis ated with a particular behaviour [118] and reveal genetic
even more daunting. correlations underlying a particular behaviour, but
If new behaviour is the result of small changes in also—since development and evolution of behaviour
regulatory regions of conserved genes, it will be diffi- and morphology influence each other—underlying par-
cult to spot the relevant ones: small changes in the ticular associations between behaviour and morphology
genome are frequently the product of drift and non- in adaptive evolution.
selective mutations. Between humans and mice, for
instance, many regulatory elements are not conserved,
and many conserved elements in regulatory regions 5. CONCLUSIONS
appear not to have a regulatory function [116]. Ideally, I have argued for the importance of keeping an eye on the
changes in behaviour should be unambiguously associ- whole phenotype while analysing individual traits. This
ated with changes at the genetic level. This is only helps for instance to recognize that key developmental
possible for experiments carried out in the same gen- elements are shared by morphology and behaviour. Be-
etic background, as in mutagenesis screens and haviour is not more plastic than morphology. It is only
selection experiments. dynamic and can be repeatedly used. Environment is a
key element of development of both traits and should
find a place in the framework of analysis of evo-devo.
(b) Mutagenesis screens and selection The tight entanglement of morphology and behaviour
experiments in development and evolution suggests that an inte-
If diversity in behaviour would be caused by a change gration of proximate and ultimate perspectives could
in the regulatory region of a gene, a small but relevant offer a better understanding of present phenotypes.
mutation in a regulatory element should affect only The functional phenotype, made of morphology and
one or few functions (e.g. in behaviour) of that gene. behaviour alike, develops and evolves as one entity.
Mutagenesis screens for behaviour have been crucial Therefore, there is only one evo-devo that includes the
to identify genes underlying important behaviours in whole functional phenotype [10].
Drosophila [117], but this method seems nowadays Since behaviour can describe ‘the way of interact-
not very popular. This may be partly due to the ing’ of elements at any level of the biological
belief that behaviour is genetically more complex hierarchy and form is the specific way—dynamic or
than morphology, because of, for example, more wide- static—in which these elements are organized, mor-
spread pleiotropy. However, there are no reasons for phology and animal behaviour could be reunited
assuming that genes affecting behaviour would display within the same framework of analysis. This frame-
more pleiotropy than genes underlying complex mor- work may be applied beyond the organism level,
phology (compare for instance [118,119]). Another such as to social groups, to understand whether prin-
reason could be that we are possibly not used to reducing ciples valid within organisms can be used to describe
complex behaviours into defined and quantifiable be- development and evolution beyond the organism
havioural patterns as we easily do with complex level [81,124]. Behaviour hence is truly the missing
morphology. New technologies can be combined with partner: not only animal behaviour at the organism
mutagenesis screens to overcome these problems, as level, needed for a better interpretation of adaptive
for instance the use of software for screening evolution but, more generally, behaviour as the way in
Phil. Trans. R. Soc. B (2011)
2064 R. C. Bertossa Introduction. Morphology and behaviour

which elements at any level of the hierarchy need to be behaviour can be addressed independently using
organized in order to obtain a specific functional form. different levels of investigation, including the DNA
The question now is understanding which are the key sequence, the gene’s position in a genetic pathway,
players at every level, how they interact and how levels spatial – temporal tissue expression and neuronal cir-
are connected. Perhaps, once having clarified this, cuit. Several examples are used to illustrate these
understanding the role of genes—i.e. whether they are points, including circadian rhythms, learning and
the major players in development and evolution—will memory, food-related behaviours and sleep. They
emerge as a natural consequence. also discuss how qualitative and quantitative compari-
sons of the behavioural phenotype, its function and the
importance of the environmental and social context
6. WHAT THE ARTICLES SAY should be used in cross-species comparisons.
While studies on behaviour development and evol- In mammals, the statistics of allometric variation in
ution have been carried out for many years, the brains within species (swine, mink, and multiple strains
treatment of behaviour within an evo-devo paradigm of laboratory mice) closely resemble phylogenetic brain
is only beginning, as reflected by the contributions variation over all mammals. Barbara Finlay, Flora
presented in the present issue. The first articles Hinz and Richard Darlington [58] argue that, first, this
[10,46,63,74] set in motion (or refresh) important dis- pattern reveals the selection of developmental parameters
cussions on general aspects of development and for brain organization robust to environmental and
evolution pertaining to behaviour. These are then niche variation at the individual level, and, second, that
more specifically addressed in the studies discussed only a restricted set of computational models of the
in the second series of articles [58,93,94,124,125]. brain can be consistent with an adaptive function for
For all those not familiar with evo-devo, the article conserved patterns of variation at within- and between-
by Paul Brakefield [10] is a very useful introduction. species scales.
He reviews some major themes and achievements of Language in animals evolved via modifications of
evo-devo, illustrating the scope of the field to reveal existing molecular and morphological hardware. Conn-
‘how the processes of development can contribute to stance Scharff & Jana Petri [93] focus on one protein,
explaining patterns of evolutionary diversification in FoxP2, which is required for language in humans, for
animal form’. In addition to stressing the exciting song learning in birds, and for motor skill learning in
potential of extending the approach of evo-devo to pat- mice. They argue that it is a good candidate to study
terns of behavioural diversification, Brakefield [10] deep homologies of molecular toolkits and neural cir-
reasons that ‘to consider the evolution of form without cuits relevant for the emergence of language. They also
taking into account its interactions with behaviour’ critically examine the (lack of) evidence for some of the
(. . .) ‘is simplistic and potentially misleading’. The claims about the uniqueness of human language.
author concludes by agreeing with some other workers Circadian systems are ubiquitous, implying an essential
in the field that understanding more about evolv- role for daily timing in evolution. Roleof Hut & Domien
ability—‘the capacity of a developmental system to Beersma [125] suggest that energy storage was crucial
evolve’—should be a key step towards answering for the earliest evolution of circadian clock systems in
many of the open questions in evo-devo. primitive photosynthesizing life forms. The modification
Studies of the evolution and the development of of ATP storage/release capacity of KaiC proteins through
behaviour take place at the ultimate and proximate KaiA suggests a daylength adaptation mechanism that
levels of analyses, respectively. There has been much may explain the global expansion of cyanobacteria. In
debate in past decades about how to (or how not to) general, different models for photoperiodic adaptation
integrate studies across these levels. Scott MacDougall- predict different selection pressures on the circadian
Shackleton [74] reviews different uses of the term ‘levels period. Hut & Beersma [125] therefore conclude that
of analysis’ and highlights how studies of function and establishing latitudinal clines in circadian tau for various
mechanism can be integrated, an approach epitomized species is crucial to reveal circadian photoperiod
by evolutionary developmental biology. adaptation mechanisms and how these may constrain
Although genetic differences can affect behaviour, responses to latitudinal expansion and global warming.
genes ultimately act through the nervous system. Paul Bee societies have fascinated humans for centuries
Katz [46] maintains that the functional organization of because of their complexity, and led to many theories
the nervous system constrains but also promotes the about the evolution of cooperative and altruistic beha-
evolvability of behaviour. He reviews evidence showing viours. Guy Bloch & Christina Grozinger [124] review
how neural mechanisms such as activity-dependent recent genomic studies on the development and evolution
plasticity and neuromodulation allow basal neural cir- of social behaviour in bees and propose a model of ‘social
cuits to be employed for different behaviours, as pathways’, modules consisting in the detection, elabor-
observed in sensory processing, motor output and ation and output of signals involved in social behaviour.
even in complex social behaviour. Katz concludes that The authors then use the model to illustrate how the
the qualities of the nervous system that enable it to pro- hormonal system and plasticity in the circadian clockwork
duce complex behaviour may also play a role in the have been modified during and contributed to the
evolvability of species-typical behaviour. evolution of bee societies.
Christopher Reaume and Marla Sokolowski [63] Taste, the sense that distinguishes between chemical
discuss how gene function, as a hierarchical biological compounds and the sensations they produce based on
phenomenon, relates to behavioural homology across contact with chemoreceptors, allows discriminating
species. They suggest that gene function homology in edible from non-edible items and is, therefore, crucial
Phil. Trans. R. Soc. B (2011)
 Introduction. Morphology and behaviour R. C. Bertossa 2065

for survival. Gabriela De Brito Sanchez & Martin 13 Jeong, S., Rebeiz, M., Andolfatto, P., Werner, T., True,
Giurfa [94] discuss the principles of taste coding in the J. & Carroll, S. B. 2008 The evolution of gene regu-
animal brain, from insects to mammals. They argue that lation underlies a morphological difference between
an essential task for a neuroscience of taste is to two Drosophila sister species. Cell 132, 783 –793.
(doi:10.1016/j.cell.2008.01.014)
determine the connectivity of taste-processing circuits in
14 Breuker, C. J., Debat, V. & Klingenberg, C. P. 2006
the central nervous system, and suggest that, beyond Functional evo-devo. Trends Ecol. Evol. 21, 488– 492.
labelled-line or across-fibre pattern coding, taste rep- (doi:10.1016/j.tree.2006.06.003)
resentations are conserved across species and seem to 15 Laubichler, M. D. & Maienschein, J. (eds) 2009 Form
relate to the hedonic value of the tastant (e.g. palatable and function in developmental evolution. Cambridge,
versus non-palatable). NY: Cambridge University Press.
16 Laubichler, M. D. 2009 Form and function in evo devo:
historical and conceptual reflections. In Form and func-
tion in developmental evolution. (eds M. D. Laubichler &
I thank D. Beersma, L. Beukeboom, P.-H. Clergeot, J. Maienschein), pp. 10–46, 1st edn. Cambridge, NY:
A. Kamping, S. Mitchell, M. Olmedo, S. Paolucci, Cambridge University Press.
T. Schwander, S. Verhulst, C. Vermeulen, L. van de Zande 17 Gilbert, S. F. 2001 Ecological developmental biology:
and three anonymous reviewers for useful discussions and developmental biology meets the real world. Dev. Biol.
comments on previous versions of the manuscript. I thank
233, 1–12. (doi:10.1006/dbio.2001.0210)
all contributors in this Special Issue for their tenaciousness
18 Gilbert, S. F. & Epel, D. 2009 Ecological developmen-
in coping with my and reviewers’ comments and apologize
with all those whose contributions could not be included in tal biology: integrating epigenetics, medicine, and
this issue. I wish to thank the following people at evolution. Sunderland, MA: Sinauer Associates.
Philosophical Transactions of the Royal Society: Joseph 19 Katz, P. S. 2006 Evolution and development of neural
James for his invitation to guest-edit the present issue; circuits in invertebrates. Curr. Opin. Neurobiol. 17,
Claire Rawlinson and Joanna Bolesworth for their patience 59–64. (doi:10.1016/j.conb.2006.12.003)
with many changes along the way. R.C.B. received support 20 Morowitz, H. J. 2002 The emergence of everything: how
with a grant from the Swiss National Science Foundation the world became complex. New York, NY: Oxford
(SNF) for prospective researchers and an ALW grant (nr. University Press.
817.02.020) from the Netherlands Organization for 21 Fentress, J. C. & McLeod, P. J. 1986 Motor patterns in
Scientific Research (NWO). development (excerpt). In The development of animal
behavior: a reader. (eds J. J. Bolhuis & J. A. Hogan),
pp. 219–244. Oxford, UK: Blackwell Publishers.
REFERENCES 22 Gottlieb, G. 1980 Development of species identification
1 Bolhuis, J. J. & Giraldeau, L.-A. (eds) 2005 The behavior in ducklings. VI: specific embryonic experience required
of animals. Oxford, UK: Blackwell Publishing. to maintain species-typical perception in Peking duck-
2 Geschwind, D. H. & Konopka, G. 2009 Neuroscience lings. In The Development of animal behavior: a reader.
in the era of functional genomics and systems biology. (eds J. J. Bolhuis & J. A. Hogan), pp. 161 –169.
Nature 461, 908 –915. (doi:10.1038/nature08537) Oxford, UK: Blackwell Publishers.
3 Ayroles, J. F. et al. 2009 Systems genetics of complex 23 Shatz, C. J. 1996 Emergence of order in visual system
traits in Drosophila melanogaster. Nat. Genet. 41, development. Proc. Natl Acad. Sci. USA 93, 602 –608.
299 –307. (doi:10.1038/ng.332) (doi:10.1073/pnas.93.2.602)
4 Dobzhansky, T. 1964 Biology, molecular and organis- 24 Marder, E. & Rehm, K. J. 2005 Development of central
mic. Am. Zool. 4, 443–452. pattern generating circuits. Curr. Opin. Neurobiol. 15,
5 West-Eberhard, M. J. 2003 Developmental plasticity and 86–93. (doi:10.1016/j.conb.2005.01.011)
evolution. Oxford, NY: Oxford University Press. 25 Goodman, C. S. & Shatz, C. J. 1993 Developmental
6 Gluckman, P. D., Beedle, A. S. & Hanson, M. 2009 mechanisms that generate precise patterns of neuronal
Principles of evolutionary medicine. 1st edn. Oxford, NY: connectivity (Review). Cell 72, 77–98. (doi:10.1016/
Oxford University Press. S0092-8674(05)80030-3)
7 Stearns, S. C., Nesse, R. M., Govindaraju, D. R. & 26 Adamo, L. et al. 2009 Biomechanical forces promote
Ellison, P. T. 2010 Evolutionary perspectives on health embryonic haematopoiesis. Nature 459, 1131–1135.
and medicine. Proc. Natl Acad. Sci. USA 107, 1691– (doi:10.1038/nature08073)
1695. (doi:10.1073/pnas.0914475107) 27 Brown, M. C., Keynes, R. J. & Lumsden, A. 2001 The
8 Pearson, R. D. 2009 Evo-Devo and the evolution of developing brain. Oxford, NY: Oxford University Press.
cancer: a hypothesis for metamorphic therapies for the 28 Bateson, P. & Hinde, R. A. 1987 developmental
cancers of prolactin-influenced tumourigenesis: with changes in sensitivity to experience. In The development
special reference to glioblastoma multiforme (GBM). of animal behavior: a reader (eds J. J. Bolhuis & J. A.
Med. Hypotheses 72, 629 –630. (doi:10.1016/j.mehy. Hogan), pp. 66–75. Oxford, UK: Blackwell Publishers.
2009.01.014) 29 Waddington, C. H. 1966 Principles of development and
9 Raff, R. A. 2007 Written in stone: fossils, genes and evo- differentiation. New York, NY: Macmillan.
devo. Nat. Rev. Genet. 8, 911–920. (doi:10.1038/nrg2225) 30 Schouenborg, J. 2002 Modular organisation and spinal
10 Brakefield, P. M. 2011 Evo-devo and accounting for somatosensory imprinting. Brain Res. Rev. 40, 80–91.
Darwin’s endless forms. Phil. Trans. R. Soc. B 366, (doi:10.1016/S0165-0173(02)00191-1)
2069 –2075. (doi:10.1098/rstb.2011.0007) 31 Polanyi, M. 1968 Life’s irreducible structure. Live
11 Muller, G. B. 2007 Evo-devo: extending the evolution- mechanisms and information in DNA are boundary
ary synthesis. Nat. Rev. Genet. 8, 943 –949. (doi:10. conditions with a sequence of boundaries above them.
1038/nrg2219) Science 160, 1308–1312. (doi:10.1126/science.160.
12 Salazar-Ciudad, I. & Jernvall, J. 2010 A computational 3834.1308)
model of teeth and the developmental origins of mor- 32 Elsasser, W. M. 1998 Reflections on a theory of organisms:
phological variation. Nature 464, 583– 586. (doi:10. holism in biology. Baltimore, MD: The Johns Hopkins
1038/nature08838) University Press.

Phil. Trans. R. Soc. B (2011)

2066 R. C. Bertossa Introduction. Morphology and behaviour

33 Nijhout, H. F. 1990 Metaphors and the role of genes in 53 Duboule, D. & Wilkins, A. S. 1998 The evolution of
development. Bioessays 12, 441–446. (doi:10.1002/ ‘bricolage’. Trends Genet. 14, 54–59. (doi:10.1016/
bies.950120908) S0168-9525(97)01358-9)
34 Goodwin, B. C. 1994 How the leopard changed its spots: the 54 Wray, G. A. 2002 Do convergent developmental mech-
evolution of complexity. New York, NY: C. Scribner’s Sons. anisms underlie convergent phenotypes? Brain Behav.
35 Pigliucci, M. 2010 Genotype–phenotype mapping and Evol. 59, 327–336. (doi:10.1159/000063566)
the end of the ‘genes as blueprint’ metaphor. Phil. 55 Sherry, D. 2005 Do ideas about function help in the
Trans. R. Soc. B 365, 557–566. (doi:10.1098/rstb. study of causation? Anim. Biol. ( formerly Netherlands
2009.0241) J. Zool.) 55, 441 –456.
36 Gottlieb, G. 1992 Individual development and evolution: 56 Nishikawa, K. C. 2002 Evolutionary convergence in
the genesis of novel behavior. New York, NY: Oxford nervous systems: insights from comparative phyloge-
University Press. netic studies. Brain Behav. Evol. 59, 240–249.
37 Gottlieb, G. 2007 Probabilistic epigenesis. Dev. Sci. 10, (doi:10.1159/000063561)
1–11. (doi:10.1111/j.1467-7687.2007.00556.x) 57 Bolhuis, J. 2005 Function and mechanism in neuroecol-
38 Westermann, G., Mareschal, D., Johnson, M. H., ogy: looking for clues. Anim. Biol. ( formerly Netherlands
Sirois, S., Spratling, M. W. & Thomas, M. S. C. 2007 J. Zool.) 55, 457 –490.
Neuroconstructivism. Dev. Sci. 10, 75–83. (doi:10. 58 Finlay, B. L., Hinz, F. & Darlington, R. B. 2011 Mapping
1111/j.1467-7687.2007.00567.x) behavioural evolution onto brain evolution: the strategic
39 Robert, J. S., Hall, B. K. & Olson, W. M. 2001 Bridging roles of conserved organization in individuals and species.
the gap between developmental systems theory and Phil. Trans. R. Soc. B 366, 2111–2123. (doi:10.1098/rstb.
evolutionary developmental biology. Bioessays 23, 2010.0344)
954 –962. (doi:10.1002/bies.1136) 59 Eisthen, H. L. 2002 Why are olfactory systems of differ-
40 Oyama, S., Griffiths, P. E. & Russell, D. G. (eds) 2001 ent animals so similar? Brain Behav. Evol. 59, 273–293.
Cycles of contingency: developmental systems and evolution. (doi:10.1159/000063564)
Cambridge, MA: The MIT Press. 60 Sih, A., Bell, A. & Johnson, J. C. 2004 Behavioral syn-
41 McPeek, M. A. 1995 Morphological evolution dromes: an ecological and evolutionary overview. Trends
mediated by behavior in the damselflies of 2 Ecol. Evol. 19, 372–378. (doi:10.1016/j.tree.2004.04.009)
communities. Evolution 49, 749–769. (doi:10.2307/ 61 Coleman, K. & Wilson, D. S. 1998 Shyness and bold-
2410328) ness in pumpkinseed sunfish: individual differences
42 Albertson, R. C., Streelman, J. T., Kocher, T. D. & are context-specific. Anim. Behav. 56, 927–936.
Yelick, P. C. 2005 From the cover: integration and (doi:10.1006/anbe.1998.0852)
evolution of the cichlid mandible: the molecular basis 62 Kozmik, Z. 2005 Pax genes in eye development and
of alternate feeding strategies. Proc. Natl Acad. evolution. Curr. Opin. Genet. Dev. 15, 430–438.
Sci. USA 102, 16 287 –16 292. (doi:10.1073/pnas. (doi:10.1016/j.gde.2005.05.001)
0506649102) 63 Reaume, C. J. & Sokolowski, M. B. 2011 Conservation
43 Abzhanov, A., Protas, M., Grant, B. R., Grant, P. R. & of gene function in behaviour. Phil. Trans. R. Soc. B 366,
Tabin, C. J. 2004 Bmp4 and morphological variation of 2100– 2110. (doi:10.1098/rstb.2011.0028)
beaks in Darwin’s finches. Science 305, 1462–1465. 64 Emery, N. J. & Clayton, N. S. 2004 The mentality of crows:
(doi:10.1126/science.1098095) convergent evolution of intelligence in corvids and apes.
44 Bakker, T. C. M. 1993 Positive genetic correlation Science 306, 1903–1907. (doi:10.1126/science.1098410)
between female preference and preferred male orna- 65 Blackledge, T. A. & Gillespie, R. G. 2004 Convergent
ment in sticklebacks. Nature 363, 255– 257. (doi:10. evolution of behavior in an adaptive radiation of Hawai-
1038/363255a0) ian web-building spiders. Proc. Natl Acad. Sci. USA
45 Emerson, S. B. & Koehl, M. A. R. 1990 The interaction 101, 16 228 –16 233. (doi:10.1073/pnas.0407395101)
of behavioral and morphological change in the evolution 66 Wagner, G. P. 2007 The developmental genetics of
of a novel locomotor type—flying frogs. Evolution 44, homology. Nat. Rev. Genet. 8, 473 –479. (doi:10.1038/
1931–1946. (doi:10.2307/2409604) nrg2099)
46 Katz, P. S. 2011 Neural mechanisms underlying the 67 Wray, G. A. & Abouheif, E. 1998 When is homology
evolvability of behaviour. Phil. Trans. R. Soc. B 366, not homology? Curr. Opin. Genet. Dev. 8, 675–680.
2086–2099. (doi:10.1098/rstb.2010.0336) (doi:10.1016/S0959-437X(98)80036-1)
47 Chiel, H. J. & Beer, R. D. 1997 The brain has a body: 68 Abouheif, E., Akam, M., Dickinson, W. J., Holland, P.
adaptive behavior emerges from interactions of nervous W., Meyer, A., Patel, N. H., Rudolf, A. R., Louise
system, body and environment. Trends Neurosci. 20, Roth, V. & Gregory, A. W. 1997 Homology and devel-
553 –557. (doi:10.1016/S0166-2236(97)01149-1) opmental genes. Trends Genet. 13, 432–433. (doi:10.
48 Parker, G. A. & Smith, J. M. 1990 Optimality theory in 1016/S0168-9525(97)01271-7)
evolutionary biology. Nature 348, 27– 33. (doi:10.1038/ 69 Abouheif, E. 1997 Developmental genetics and hom-
348027a0) ology: a hierarchical approach. Trends Ecol. Evol. 12,
49 Gittleman, J. L. 1989 The comparative approach in 405 –408. (doi:10.1016/S0169-5347(97)01125-7)
ethology: aims and limitations. In Perspectives in ethology: 70 Gehring, W. J. & Ikeo, K. 1999 Pax 6—mastering eye
vol. 8, Whither ethology? (eds P. P. G. Bateson & P. H. morphogenesis and eye evolution. Trends Genet. 15,
Klopfer), pp. 55–83. New York, NY: Plenum Press. 371 –377. (doi:10.1016/S0168-9525(99) 01776-X)
50 Gould, S. J. & Vrba, E. S. 1982 Exaptation; a missing 71 Hall, B. K. (ed.) 1994 Homology: the hierarchical basis of
term in the science of form. Paleobiology 8, 4 –15. comparative biology. 1st edn. San Diego, CA: Academic
51 Brakefield, P. M. 2006 Evo-devo and constraints on Press.
selection. Trends Ecol. Evol. 21, 362–368. (doi:10. 72 Minelli, A. 1998 Molecules, developmental modules,
1016/j.tree.2006.05.001) and phenotypes: a combinatorial approach to homo-
52 Wilkins, A. S. 2007 Colloquium papers: between ‘design’ logy. Mol. Phylogenet. Evol. 9, 340–347. (doi:10.1006/
and ‘bricolage’: genetic networks, levels of selection, mpev.1997.0490)
and adaptive evolution. Proc. Natl Acad. Sci. USA 104, 73 Hall, B. K. 2003 Descent with modification: the unity
8590–8596. (doi:10.1073/pnas.0701044104) underlying homology and homoplasy as seen through

Phil. Trans. R. Soc. B (2011)

 Introduction. Morphology and behaviour R. C. Bertossa 2067

an analysis of development and evolution. Biol. Rev. 93 Scharff, C. & Petri, J. 2011 Evo-devo, deep homology
Camb. Phil. Soc. 78, 409 –433. (doi:10.1017/ and FoxP2: implications for the evolution of speech
S1464793102006097) and language. Phil. Trans. R. Soc. B 366, 2124–2140.
74 MacDougall-Shackleton, S. A. 2011 The levels of (doi:10.1098/rstb.2011.0001)
analysis revisited. Phil. Trans. R. Soc. B 366, 2076– 94 de Brito Sanchez, G. & Giurfa, M. 2011 A comparative
2085. (doi:10.1098/rstb.2010.0363) analysis of neural taste processing in animals. Phil.
75 Ryan, M. J. 2005 The evolution of behaviour, and inte- Trans. R. Soc. B 366, 2171–2180. (doi:10.1098/rstb.
grating it towards a complete and correct understanding 2010.0327)
of behavioural biology. Anim. Biol. 55, 419–439. 95 Briggman, K. L. & Kristan, W. B. 2008 Multifunctional pat-
(doi:10.1163/157075605774841012) tern-generating circuits. Annu. Rev. Neurosci. 31, 271–294.
76 Cap, H., Deleporte, P., Joachim, J. & Reby, D. (doi:10.1146/annurev.neuro.31.060407.125552)
2008 Male vocal behavior and phylogeny in deer. 96 Katz, P. S. & Harris-Warrick, R. M. 1999 The evolution
Cladistics 24, 917– 931. (doi:10.1111/j.1096-0031. of neuronal circuits underlying species-specific behav-
2008.00223.x) ior. Curr. Opin. Neurobiol. 9, 628 –633. (doi:10.1016/
77 Scholes, E. 2008 Evolution of the courtship phenotype S0959-4388(99)00012-4)
in the bird of paradise genus Parotia (Aves: Paradisaei- 97 Wray, G. A. 2007 The evolutionary significance of cis-
dae): homology, phylogeny, and modularity. Biol. J. regulatory mutations. Nat. Rev. Genet. 8, 206– 216.
Linn. Soc. 94, 491 –504. (doi:10.1111/j.1095-8312. (doi:10.1038/nrg2063)
2008.01012.x) 98 Carroll, S. B. 2008 Evo-devo and an expanding evolution-
78 Lorenz, K. 1937 Über die Bildung des Instinktbegriffes. ary synthesis: a genetic theory of morphological evolution.
Naturwiss 25, 324 –331. (doi:10.1007/BF01774269) Cell 134, 25–36. (doi:10.1016/j.cell.2008.06.030)
79 Verni, F. & Gualtieri, P. 1997 Feeding behaviour in 99 Hoekstra, H. E. & Coyne, J. A. 2007 The locus of evol-
ciliated protists. Micron 28, 487–504. (doi:10.1016/ ution: evo devo and the genetics of adaptation. Evol.
S0968-4328(97)00028-0) Int. J. Org. Evol. 61, 995 –1016.
80 Erwin, D. H. & Davidson, E. H. 2009 The evolution of 100 Craig, L. R. 2009 Defending evo-devo: a response to
hierarchical gene regulatory networks. Nat. Rev. Genet. Hoekstra and Coyne. Phil. Sci. 76, 335 –344. (doi:10.
10, 141– 148. (doi:10.1038/nrg2499) 1086/649808)
81 Hamilton, A. L. 2009 Toward a mechanistic evo devo. 101 Chan, Y. F. et al. 2010 Adaptive evolution of pelvic
In Form and function in developmental evolution (eds M. reduction in sticklebacks by recurrent deletion of a
D. Laubichler & J. Maienschein), pp. 213–224. Pitx1 enhancer. Science 327, 302 –305. (doi:10.1126/
Cambridge, NY: Cambridge University Press. science.1182213)
82 Toth, A. L. & Robinson, G. E. 2007 Evo-devo and the 102 Shapiro, M. D., Marks, M. E., Peichel, C. L., Blackman,
evolution of social behavior. Trends Genet. 23, 334– 341. B. K., Nereng, K. S., Jonsson, B., Schluter, D. & Kingsley,
(doi:10.1016/j.tig.2007.05.001) D. M. 2004 Genetic and developmental basis of evol-
83 Davidson, E. H. & Erwin, D. H. 2006 Gene regulatory utionary pelvic reduction in threespine sticklebacks.
networks and the evolution of animal body Nature 428, 717–723. (doi:10.1038/nature02415)
plans. Science 311, 796 –800. (doi:10.1126/science. 103 Cretekos, C. J., Wang, Y., Green, E. D., Martin, J. F.,
1113832) Rasweiler, J. J. T. & Behringer, R. R. 2008 Regulatory
84 Olson, E. N. 2006 Gene regulatory networks in the divergence modifies limb length between mammals.
evolution and development of the heart. Science 313, Genes Dev. 22, 141–151. (doi:10.1101/gad.1620408)
1922 –1927. (doi:10.1126/science.1132292) 104 Tishkoff, S. A. et al. 2007 Convergent adaptation of
85 Pueyo, J. I. & Couso, J. P. 2005 Parallels between the human lactase persistence in Africa and Europe. Nat.
proximal–distal development of vertebrate and arthro- Genet. 39, 31–40. (doi:10.1038/ng1946)
pod appendages: homology without an ancestor? Curr. 105 Sokolowski, M. B. 2001 Drosophila: genetics meets be-
Opin. Genet. Dev. 15, 439– 446. (doi:10.1016/j.gde. haviour. Nat. Rev. Genet. 2, 879 –890. (doi:10.1038/
2005.06.007) 35098592)
86 Pires-daSilva, A. & Sommer, R. J. 2003 The evolution 106 Redies, C. & Puelles, L. 2004 Central nervous system
of signalling pathways in animal development. Nat. development: from embryonic modules to functional
Rev. Genet. 4, 39–49. (doi:10.1038/nrg977) modules. In Modularity in development and evolution
87 Lemons, D. & McGinnis, W. 2006 Genomic evolution (eds G. Schlosser & G. P. Wagner), pp. 154 –182.
of Hox gene clusters. Science 313, 1918–1922. Chicago, IL: University of Chicago Press.
(doi:10.1126/science.1132040) 107 Goulding, M. 2009 Circuits controlling vertebrate loco-
88 Edwards, D. H. & Kravitz, E. A. 1997 Serotonin, social motion: moving in a new direction. Nat Rev Neurosci.
status and aggression. Curr. Opin. Neurobiol. 7, 10, 507 –518. (doi:10.1038/nrn2608)
812 –819. (doi:10.1016/S0959-4388(97)80140-7) 108 Young, L. J., Nilsen, R., Waymire, K. G., MacGregor,
89 Alberini, C. M. 1999 Genes to remember. J. Exp. Biol. G. R. & Insel, T. R. 1999 Increased affiliative response
202, 2887 –2891. to vasopressin in mice expressing the V1a receptor from
90 Denes, A. S., Jekely, G., Steinmetz, P. R., Raible, F., a monogamous vole. Nature 400, 766 –768. (doi:10.
Snyman, H., Prud’homme, B., Ferrier, D. E. K., 1038/23650)
Balavoine, G. & Arendt, D. 2007 Molecular architec- 109 Prabhakar, S., Noonan, J. P., Paabo, S. & Rubin, E. M.
ture of annelid nerve cord supports common origin of 2006 Accelerated evolution of conserved noncoding
nervous system centralization in bilateria. Cell 129, sequences in humans. Science 314, 786. (doi:10.1126/
277 –288. (doi:10.1016/j.cell.2007.02.040) science.1130738)
91 Arendt, D., Denes, A. S., Jekely, G. & Tessmar-Raible, 110 Fisher, S. E. & Marcus, G. F. 2006 The eloquent ape:
K. 2008 The evolution of nervous system centralization. genes, brains and the evolution of language. Nat. Rev.
Phil. Trans. R. Soc. B 363, 1523–1528. (doi:10.1098/ Genet. 7, 9–20. (doi:10.1038/nrg1747)
rstb.2007.2242) 111 Rilling, J. K., Glasser, M. F., Preuss, T. M., Ma, X., Zhao,
92 Scharff, C. & Haesler, S. 2005 An evolutionary perspective T., Hu, X. & Behrens, T. E. J. 2008 The evolution of the
on FoxP2: strictly for the birds? Curr. Opin. Neurobiol. 15, arcuate fasciculus revealed with comparative DTI. Nat.
694–703. (doi:10.1016/j.conb.2005.10.004) Neurosci. 11, 426–428. (doi:10.1038/nn2072)

Phil. Trans. R. Soc. B (2011)

2068 R. C. Bertossa Introduction. Morphology and behaviour

112 Certel, S. J., Savella, M. G., Schlegel, D. C. & Kravitz, bristle number in Drosophila melanogaster. Genetics 139,
E. A. 2007 Modulation of Drosophila male behavioral 1273–1291.
choice. Proc. Natl Acad. Sci. USA 104, 4706–4711. 120 Chronis, N., Zimmer, M. & Bargmann, C. I. 2007
(doi:10.1073/pnas.0700328104) Microfluidics for in vivo imaging of neuronal and be-
113 Carroll, S. B. 2005 Endless forms most beautiful: the new havioral activity in Caenorhabditis elegans. Nat. Methods
science of evo devo and the making of the animal kingdom. 4, 727 –731. (doi:10.1038/nmeth1075)
New York, NY: Norton. 121 Branson, K., Robie, A. A., Bender, J., Perona, P. &
114 Canestro, C., Yokoi, H. & Postlethwait, J. H. 2007 Dickinson, M. H. 2009 High-throughput ethomics in
Evolutionary developmental biology and genomics. Nat. large groups of Drosophila. Nat. Methods 6, 451–477.
Rev. Genet. 8, 932–942. (doi:10.1038/nrg2226) (doi:10.1038/nmeth.1328)
115 Boguski, M. S. & Jones, A. R. 2004 Neurogenomics: at 122 Anholt, R. R. & Mackay, T. F. 2004 Quantitative
the intersection of neurobiology and genome sciences. genetic analyses of complex behaviours in Droso-
Nat. Neurosci. 7, 429 –433. (doi:10.1038/nn1232) phila. Nat. Rev. Genet. 5, 838 –849. (doi:10.1038/
116 Clark, A. G. 2006 Genomics of the evolutionary pro- nrg1472)
cess. Trends Ecol. Evol. 21, 316 –321. (doi:10.1016/j. 123 Stapley, J. et al. 2010 Adaptation genomics: the next
tree.2006.04.004) generation. Trends Ecol. Evol. 25, 705–712. (doi:10.
117 Hall, J. C. 2003 A neurogeneticist’s manifesto. 1016/j.tree.2010.09.002)
J. Neurogenet. 17, 1–90. 124 Bloch, G. & Grozinger, C. M. 2011 Social molecular
118 Toma, D. P., White, K. P., Hirsch, J. & Greenspan, R. J. pathways and the evolution of bee societies. Phil.
2002 Identification of genes involved in Drosophila Trans. R. Soc. B 366, 2155–2170. (doi:10.1098/rstb.
melanogaster geotaxis, a complex behavioral trait. 2010.0346)
Nat. Genet. 31, 349 –353. 125 Hut, R. A. & Beersma, D. G. M. 2011 Evolution of
119 Long, A. D., Mullaney, S. L., Reid, L. A., Fry, J. D., time-keeping mechanisms: early emergence and adap-
Langley, C. H. & Mackay, T. F. C. 1995 High resol- tation to photoperiod. Phil. Trans. R. Soc. B 366,
ution mapping of genetic factors affecting abdominal 2141–2154. (doi:10.1098/rstb.2010.0409)

Phil. Trans. R. Soc. B (2011)

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