Evol Ecol (2010) 24:571–583

DOI 10.1007/s10682-009-9336-y

ORIGINAL PAPER

Behavioural plasticity: an interaction between evolution

and experience

Frederic Mery • James G. Burns

Received: 31 March 2009 / Accepted: 22 October 2009 / Published online: 26 November 2009
Ó Springer Science+Business Media B.V. 2009

Abstract Animals adjust their behaviour in response to complex environmental condi-

tions. This form of plasticity requires the formation of association between information and
an appropriate behavioural response. Such a connection is the result of a complex inter-
action between evolutionary pre-programmed cue-response behaviour (innate behavioural
response) and cumulated lifetime experience (learning). The evolution of learning and
innate behavioural responses is likely to depend on their respective fitness costs and
benefits. However, as natural selection will indirectly affect each form through global
behavioural plasticity, it is critical to understand how each form interacts with the other.
The inclusion of innate behavioural plasticity and learning in behaviour is likely to result in
more than the mere sum of each plastic form. In this review we investigate the costs and
benefits of learning and innate behavioural responses and the effect of one on the other in
their evolution. We highlight the need for more explicit study of the interaction between
innate behavioural response and learning in natural systems for a better understanding of
behavioural plasticity.

Keywords Information
Costs
Benefits
Environmental heterogeneity

Introduction

Organisms have the ability to vary their behaviour in response to environmental changes;
this behavioural plasticity involves a large spectrum of behavioural mechanisms and
properties that are dependent on many physiological patterns. Although behavioural
plasticity is usually associated with neuronal plasticity, it may also include other changes.
In fact, each occurrence of behavioural modification induced by environmental factors

F. Mery (&)
J. G. Burns

Laboratoire Evolution Génome et Spéciation, UPR9034, Centre National de la Recherche Scientifique
and Université Paris-Sud 11, 91198 Gif sur Yvette Cedex, France
e-mail: frederic.mery@legs.cnrs-gif.fr

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through integration of sensory input could be associated with behavioural plasticity

(e.g. chemotaxis in bacteria, Bourret and Stock 2002). How such information becomes
associated with a behavioural response is central to understanding animal adaptation. We
will concentrate on two forms of behavioural plasticity and investigate their relationship
and evolution: innate behavioural responses and learning. Innate behavioural response
occurs when the modification of behaviour in response to environmental factors is the
result of evolution at the population scale over multiple generations; that is, a predeter-
mined phenotypic trait is produced in response to a predetermined environmental stimulus.
Learning occurs when a modification of behaviour is produced by experience within the
lifetime of an individual (Dukas 1998a; Papaj and Prokopy 1989; Shettleworth 1998).
Innate behavioural response and the ability to learn are both the result of evolution and
exhibit natural genetic diversity. For example, there is strong genetic variation in innate
predator avoidance among Daphnia magna clones (de Meester 1996), while learning
ability has been shown to differ among closely related species (Smid et al. 2007; Roudez
et al. 2008) and among populations of the same species (Girvan and Braithwaite 1998;
Pravosudov and Clayton 2002).
Of course, it is a false dichotomy to separate behaviours into categories of either innate
or learned; behaviour is a result of an interaction among these processes and there is no
continuum between purely learned behaviour and purely innate ones. In most cases, ani-
mals are born with a certain innate predisposition to perform a behaviour which will be
more or less modified by experience. The relative effect of learning on behaviour is likely
to depend on the specific task to be performed or on the species considered. Animals have
evolved predispositions to pay attention to some stimuli more than others; that is, innate
behavioural responses may simply focus attention on cues most relevant to the evolu-
tionary history of the animal (Garcia and Koelling 1966; Domjam and Wilson 1972; Bolles
1970). Also, animals may routinely perform certain behaviours in natural learning con-
texts. For instance, Breland’s (1961) famous coin-washing racoons habitually performed a
natural ‘‘food’’ washing behaviour, even though they were only rewarded for learning to
pick up coins and deposit them in a container. Natural selection may thus act on both innate
behavioural responses and learning independently to optimize behaviour. This optimiza-
tion is likely to depend on the respective costs and benefits of these two information
processes. Here we present some evidence for the potential benefits, costs, and constraints
of innate behavioural responses and learning, and then discuss how the evolution of each
process may depend on environmental conditions.

Benefits of learning versus innate behavioural responses

The evolution of any phenotypic trait is thought to result from trade-offs between the
fitness costs and benefits associated with it (Stearns 1992). Different environmental con-
ditions can alter these fitness trade-offs and lead to phenotypic variation among species and
populations. However, environments also tend to be highly variable, such that no single
behavioural phenotype is consistently optimal. These dynamic conditions will favour
behavioural plasticity as a means of tracking environmental change. The requirements for
the evolution of behavioural plasticity are: (1) environmental heterogeneity, (2) reliable
cues, (3) benefits that outweigh the costs of plasticity, and (4) a genetic basis to plasticity
(Berrigan and Scheiner 2004).
A long history of theoretical modelling on the evolution of plasticity has described how
spatial or temporal heterogeneity may favour different forms of plasticity. When an

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organism faces spatial and/or temporal heterogeneity during its lifetime, reversible plas-
ticity is favoured. Tadpoles exposed to predators reduce activity levels and resume activity
when predators are removed (Van Buskirk 2002), demonstrating the advantages of rapid,
reversible innate behavioural responses in response to temporal changes in the selective
environment. However, if the heterogeneity occurs between generations or exceeds the
organism’s dispersal capabilities, then irreversible plasticity may be favoured (Moran
1992). The development of social preferences in young animals for their parents (an
environmental factor that changes between generations), or filial imprinting, is an example
of learning that, although flexible in the lab (Bolhuis 1991), is almost irreversible in nature.
Yet, individuals usually do not over-commit to cues. A stimulus encountered only once
usually generates a semi-stabilized memory, whereas information that has been encoun-
tered on multiple, independent occasions is stored in consolidated long-term memory (e.g.
Isabel et al. 2004). Thus, learning and innate behavioural plasticity can both be reversible
or irreversible. Innate behavioural responses, though, can only evolve over generations at
the population level (via reproduction), while a learned response is formed within the
lifetime of an individual. Environmental heterogeneity is therefore likely to play a key role
in the relative benefits of these two strategies. Innate behavioural responses may be ben-
eficial when environmental conditions are spatially stable and temporally variable over the
long term, but regular over the short-term, whereas learning may be beneficial under the
opposite circumstances (Stephens 1991).
In contrast to innate behavioural responses, learning has an additional level of flexibility
that allows an individual to change either the stimulus it responds to or the response to the
same stimulus (Dukas 1998b). The same stimulus may also be associated with a different
behaviour depending on contextual parameters. In classical conditioning experiments, the
timing between presentation of the unconditioned stimulus and the conditioned stimulus
can lead to opposite behaviours (Moscovitch and Lolordo 1968; Shettleworth 1998). Such
flexibility may provide some key advantages for learning as it allows the individual to be
adapted to the local environmental conditions. Furthermore, innate behavioural responses
are likely to be exploited by parasites or predators. Cuckoo chicks exploit the innate
feeding behaviour of the reed warbler adult by mimicking the begging call of their host
(Davies et al. 2006).
The environmental heterogeneity associated with predation risk can serve as an example
of the flexibility added by learning. A rapid, innate anti-predator behavioural response is
likely to be an efficient means of avoiding injuries or death in initial encounters with
predators. However, experience may enhance the ability to recognize predators. In aquatic
environments, reception of chemical stimuli released by injured prey (alarm cues) and
predators (kairomones) is the primary sensory mode by which most taxa gather information
about the threat of predation (Kats and Dill 1998). Naı̈ve prey animals often respond to
alarm chemicals released by injured conspecifics (Magurran 1986). A number of studies
have shown that naı̈ve prey may fail to recognize predators based on kairomones alone, but
will learn to associate kairomones with predation risk when they are presented in con-
junction with alarm cues (Jachner 2001). Experience may also affect the type of anti-
predator response used by prey. Prey are often confronted with multiple types of predators,
each with unique foraging modes, and prey respond with a range of defensive strategies,
each best suited for use against a particular predator (Relyea 2001; Turner et al. 1999).
Given that there is often incomplete or unreliable information regarding predator identity
in the wild, the selection of an antipredator strategy should be informed by recent
experience.

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Costs of learning versus innate behavioural responses

The existence of variation in behavioural plasticity among closely related species, among
populations of the same species, or between the sexes, indicates that the evolution of
behavioural plasticity is likely dependent on a balance between its benefits and its costs.
Costs of behavioural plasticity have long been hypothesized (DeWitt et al. 1998; Dukas
1999; Johnston 1982), but direct experimental evidence is still scarce (Pigliucci 2005).

Costs of being naı̈ve

Behavioural plasticity requires a large behavioural repertoire and selection, using envi-
ronmental information as a guide, of an adaptive behavioural response. During learning, this
selection process is usually performed through trial-and-error, which subjects an animal to a
period of suboptimal behaviour. This is the oft-mentioned ‘‘cost of being naı̈ve’’.
Even those employing innate behavioural responses can suffer a kind of cost of being
naı̈ve. The evolution of an innate behavioural response, to some potential optimum, can
only be observed over several generations and a mismatch between current environmental
conditions and the behavioural response may perpetuate. For example, Sasaki and co-
workers (2009) found an association between recent intense hunting pressure and the
evolution of escape behaviour in the snake Gloydius blomhoffii. Population size dropped
significantly after hunting commenced; the population size stabilized after escape behaviour
evolved. There was thus a costly time lag between change in environmental conditions and
evolution of adapted behavioural responses. However, now that an adaptive response has
been established, individuals do not have to pay this cost anymore (assuming stable envi-
ronmental conditions). Thus, before an innate behavioural response reaches fixation (or
stable level) within a population, many individuals will not behave in particularly adaptive
ways in comparison to populations that have already responded to the selective pressure.
Naivety costs have been proposed to be much more important in learning because every
generation the behavioural responses must be relearned. This requires time (and the
associated loss of opportunities), loss of energy intake, and errors that can be potentially
risky for the individual. Examples include the practice time bumblebees need before they
can handle a novel flower efficiently (Laverty and Plowright 1988), and mortality of bird
fledglings due to inexperience in food gathering (Johnston 1982; Sullivan 1988).
One should note that this cost of being naı̈ve is not directly related to learning per se, but
rather to the ability to display a large behavioural repertoire before learning occurs [‘‘cost
of being a generalist’’ as mentioned by Dall and Cuthill (1997)]. That is, having many
potential options at one’s disposal increases the costs—through a prolonged trial and error
process—of coming to final decision. A slow learner pays higher costs (in terms of time
and number of errors) than a fast learner. Increasing learning ability should decrease these
costs. Laverty and Plowright (1988) compared the flower handling skill of specialist and
generalist bumblebee species. With no previous experience, the specialist species quickly
located the nectar but the generalists performed poorly and only mastered the task after
several visits. Without any learning, the generalist species would pay error costs over and
over again, but learning allows them to fine tune their behaviour and reduce these costs.
Similarly, the butterfly Pieris rapae can learn to improve its oviposition-site search. In a
recent experiment, Snell-Rood and Papaj (2009) showed a positive correlation between
learning ability and efficiency of foraging that suggests that learning decreases the costs of
being naive. It makes then little sense to directly associate costs of naivety with learning
since they are inversely related. The costs of being naive should be more associated with

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the innate ability to perform or not a large behavioural repertoire; this innate ability is not
necessarily linked to learning speed or efficiency. Improving learning ability is actually a
means to reducing the cost of being naı̈ve. To understand whether animals should evolve
innate specialization for a task or remain as generalists, it is therefore important to know
how much an animal must invest to learn it. The costs of learning are more directly related
to the constitutive and induced costs of being able to learn.

Constitutive and induced costs

Costs of behavioural plasticity may be incurred whether or not plasticity is exhibited. Such
effects may be due to the development and maintenance costs of the neural structures
involved in learning and memory (Dukas 1999) or maintenance costs of sustaining the
sensory and response pathways that induce plastic responses. As natural populations face a
world with limited resources, the extra energy expenditure should be reflected in reduction
of survival or fecundity. Hence, the capability for plasticity is expected to show evolu-
tionary trade-offs with other fitness-related traits. Mery and Kawecki (2002) showed that
fruit flies selected for improved learning ability had reduced larval competitive ability even
when their learning and memory abilities were not challenged.
Learning and innate behavioural responses may both strongly depend on the develop-
ment and maintenance of the brain. Based on its mass, and compared to other tissues in the
body, nervous tissue uses a disproportionate amount of energy (Laughlin 2001; Laughlin
et al. 1998), primarily to conduct action potentials and maintain resting potentials (Attwell
and Laughlin 2001). However, we are aware of no specific comparison of energy costs paid
by large-brained versus small-brained individuals within the same species. The experi-
mental generation of genetic variation in brain size, or better yet specific brain structures
with identified functions (Healy and Rowe 2007), through selection experiments would be
valuable; attempts so far been stymied because selection for brain weight was accompanied
by a plethora of correlated responses (Fuller 1979; Jensen 1979). There is, though, some
comparative evidence for the costs of brain tissue trading off with other fitness-related
traits (brain size and muscle mass: Isler and van Schaik 2006; brain size and life history
traits: Iwaniuk and Nelson 2003; Barrickman et al. 2008). For example, bat species with
promiscuous females have relatively smaller brains than do species with females exhibiting
mate fidelity (Pitnick et al. 2006), which the authors hypothesize is due to a trade-off
between investment in testes versus in brains, both metabolically expensive tissues. Also,
gestation time is positively correlated to brain weight in placental mammals (Sacher and
Staffeldt 1974) and might be an example of a constitutive cost of behavioural plasticity.
Other indirect evidence for the costs of brain tissue comes from instances when brain tissue
or activity is reduced. For instance, in some ants the switch from forager or winged virgin
queen to a reproductive stage with a reduced behavioural repertoire is accompanied by a
reduction in brain volume (Gronenberg and Liebig 1999; Julian and Gronenberg 2002).
Also, teenage girls trained to play a problem-solving computer game, Tetris, showed
increased cortical thickness in some brain areas after 3 months, but also had decreased
brain activity in other areas (Haier et al. 2009).
A question remains as to whether increased brain size results in greater behavioural
plasticity (Burns and Rodd 2008; Marino 2005; Sol et al. 2005). There is evidence from
comparative studies; for instance, there is a strong positive relationship between behav-
ioural repertoire size and encephalization among mammals (Changizi 2003). Also, the size
of the hippocampus has been found to be positively correlated with spatial learning ability
among species (Biegler et al. 2001), among genotypes within species (Crusio et al. 1993),

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and between the sexes (Jacobs et al. 1990). Evidence is accumulating that large brains
facilitate the development of novel behaviours that may help to deal with new ecological
challenges (Sol 2009). These structures are however, likely to be energetically costly
(Sokoloff 1960; Dukas 1999). Also, seasonal variation of brain size has been observed in
some bird species, such as free-ranging black-capped chickadees, that show strong neu-
ronal replacement in fall when the acquisition of new spatial memories might be beneficial
for food storing (reviewed in Sherry and Hoshooley 2009). Similarly, enriched animals
(raised in larger, more spatially or socially complex environments) tend to have larger
brain structures, higher rates of neurogenesis and/or greater learning ability than deprived
animals (Rosenzweig and Bennett 1996; van Praag et al. 2000). This seasonal and envi-
ronmentally-induced variation indicates that there may be constitutive costs of neural
structure maintenance, and that variance is generated by the demand for learning and for an
efficient strategy to reduce costs when learning is less needed. In a recent study by Snell-
Rood and co-workers (2009), comparisons among butterfly (Pieris rapae) families showed
a positive correlation between host finding learning capacities and mushroom body size at
emergence and an increase of the adult brain size followed specifically by learning
experience. In honeybees, long-term memory formation is associated with increased vol-
ume in specific brain glomeruli (Hourcade et al. 2009). It is not clear, however, whether
such plasticity in brain size results in improved learning ability or is a consequence of
memory storage. These data do suggest that constitutive variation in brain size may relate
to variation in learning ability but may also induce constitutive costs which are reduced by
experience-specific changes in brain size.
Compared to innate behavioural responses, the process of learning has been shown to
induce important neurobiological and morphological reorganization. The use and modifi-
cation of neural tissue during the learning process are some of the induced costs of learning
(e.g. Mery and Kawecki 2004b). The energetic costs of learning have not been directly
demonstrated, but Laughlin and co-workers (Laughlin 2001; Niven et al. 2007) have
measured the metabolic cost of information processing in a photoreceptor of the fly
compound eye. They found the existence of a trade-off between energy consumption and
neuronal performance. Such energy expenditure might represent a significant cost reflected
in other fitness traits. For instance, consolidation of information into long-term memory
reduces the resistance of adult Drosophila to stress imposed by absence of food and water
(Mery and Kawecki 2005).
It is possible that the differences in the costs of maintenance of the sensory input, motor
patterns and neuronal integrity of innate behavioural responses and learning are not so
great. Even if behavioural responses can occur without any neuronal structures, it is not
clear whether learning requires, on average, a bigger brain. Neural plasticity is a basic
property of any central nervous system and does not necessarily require more neurons than
innate behavioural responses. During learning, the brain integrates information to create
new associations, while in innate behavioural responses the brain will create predefined
association. While the consensus is that there are additional induced costs to learning and
remembering, we lack direct experimental evidence for their magnitude.

Constraints on learning and response by evolution

Two factors are particularly crucial for learning to occur. First, in order to be able to
modify their behaviour according to environmental conditions, animals must obtain direct
information about the consequence of an action on their state or fitness. The establishment

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of a relationship between a specific action and its consequence might be constrained by the
delay between the two or by a lack of direct consequence on the individual’s state. Many
learning experiments have shown that most learning does not occur with delays longer than
a few seconds [with the well-studied exception of taste-aversion learning (Garcia and
Koelling 1966)]. For instance, Drosophila cannot learn to associate an odorant with an
electric shock in a classical conditioning experiment when both are separated by more than
60s (Tanimoto et al. 2004). Second, animals live in a complex world where some infor-
mation is relevant and some is not. They must be able to extract and select which envi-
ronmental cue, if any, predicts the consequence of an action. This might be one of the
major constraints on learning and certainly increases the time required to master a task.
The evolution of learning has led to the development of different properties and mecha-
nisms allowing an animal to select cues and to track environmental complexity. When
learning, animals are not equally sensitive to all cues but more prone to pay attention to
some and neglect others. Food aversion learning experiments suggests that some stimuli
are more associable than others; these studies show that many animals are more likely to
associate intestinal illness with gustatory (or olfactory) stimuli than with external stimuli
(sound or light) (Garcia and Koelling 1966). These results were first viewed as constraints
on learning, but the predisposition to respond to certain cues is likely to be an evolutionary
adaptation to select for more relevant cues while learning (Shettleworth 1998). For
instance, specialized forms of learning are associated with species life history. The vampire
bat, Desmondus rotundus, is the only animal known that is unable to readily form learned
taste aversions (Ratcliffe et al. 2003). However, in its natural environment, its food—the
blood of live animals—is always fresh and cannot be poisonous or the donor would not be
alive. Imprinting by young animals on, typically, their mother is another classic example.
The dynamics of learning (e.g. the amount of experience required, the nature of cues to
which associations are most easily made, and the affect of delay between cue and result)
are likely to differ accordingly to the type of learning, the relevance of the cues in the
environment, and the balance between the benefits and the costs of adopting a behaviour.
One should also note that predispositions may constrain the development of innovative
behaviour because associations between initially unrelated information may be ignored
even when the information becomes relevant.
The evolution of learning is based on the ability to make associations and can be
constrained by the occurrence of environmental factors. Interestingly, we see that these
constraints on learning might be relaxed by innate behavioural responses that facilitate the
detection and selection of the behavioural input and output. As learning may also allow for
the genetic accommodation of innate behavioural responses (West-Eberhard 2003), the
evolution of learning and innate behavioural responses may be highly interrelated.

Evolution of learning and innate behavioural responses

Learning ability and innate behavioural response could in principle evolve independently
under different environmental conditions. For example, populations of three-spined
sticklebacks living in ponds or in rivers show similar spatial learning abilities but different
innate attraction to spatial cues (Odling-Smee and Braithwaite 2003). Similarly, Mery and
Kawecki (2002) selected flies for improved learning ability in an oviposition site choice
test without affecting any innate behavioural response. Natural selection, though, generally
acts directly on behaviour, so will usually act indirectly on each component. Thus, the
evolution of a combination of learning and innate behavioural responses is probably a

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common process. After all, both forms usually require similar structures such as sensory
organs and neural organisation to integrate information and translate it into behaviour.
As both forms of plasticity are likely to evolve together, a question remains on how each
form interacts with the evolution of the other. Gumbert (2000) found that learned pref-
erences for certain flower colours affected latter choices between novel, differently col-
oured flowers only when the dominant wavelength of one of the new colours could be
generalized to the trained flower colour. Otherwise, innate colour preferences predomi-
nated. In Drosophila, males initiate an innate rigid and complex sequence of courtship
activity in response to conspecific females emitting sex pheromones. However, males that
experienced courtship and rejection by heterospecific females exhibited significantly lower
levels of heterospecific courtship and mating compared with those of inexperienced males
(Dukas 2008) suggesting the importance of the interaction between innate behavioural
response and learning in many aspects of animal fitness and species evolution. The evo-
lution of innate behavioural responses may facilitate learning by predisposing animals to
learn specific associations or inhibit the possibility to create new original associations. On
the other hand, learning may allow an individual to adjust its behaviour irrespective of its
innate behavioural response. This masking effect should make natural selection on the
innate, heritable component of the behavioural response less effective, slowing down its
evolution (Robinson and Dukas 1999; Papaj 1994). In contrast, a simulation model by
Hinton and Nowlan (1987) suggested that in a novel environment learning might accelerate
the evolution of the innate component towards the optimum. A similar prediction has been
obtained in artificial intelligence models (Belew 1989; Ackley and Littman 1990; Mayley
1997). These models provide some formal underpinning for the old verbal arguments that
learning may accelerate evolution (Baldwin 1896; Morgan 1896). Quantitative genetic
models making more general assumptions about the fitness function (Anderson 1995;
Ancel 2000), though, suggest that the conditions under which learning may facilitate
evolution are highly restricted.
Mery and Kawecki (2004a) tested how selection for an innate preference could interact
with the opportunity to learn. In their selection experiment on innate preference for two
different substrates (orange and pineapple) for oviposition in Drosophila melanogaster,
two additional treatments also allowed the flies to use previous aversion learning experi-
ence to select an oviposition. Of primary importance was the result that the opportunity to
learn facilitated the evolution of an innate preference for pineapple, but slowed selection
for an innate preference for orange. The devil may be in the details for what conditions lead
selection in the direction of facilitating evolution of an innate behavioural response versus
its hindrance. There does not seem to be a solution to this puzzle on the near horizon.

Cultural transmission as a replacement for innate behavioural plasticity?

This review has concentrated on the distinction between two forms of plasticity in which
individuals modify their behaviour independently of other individuals. However, modifi-
cation of behaviour can also occur after observation of or interaction with other animals
(Heyes 1994). Compared to individual learning, which requires a trial and error period in
every generation, social learning can result in stable tradition transmission across gener-
ations. Bird song imitation is an example of stable cultural transmission (Podos et al. 2004;
Grant and Grant 1996) that allows the long-term maintenance of species recognition and
mate choice, and may even contribute to increased rates of allopatric speciation (Lachlan
and Servedio 2004). Like an innate behavioural response, a culturally transmitted trait may

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evolve between generations through copying inaccuracies and selection (Podos et al.
2004), and thus may be favoured under stable environmental conditions. This may result in
individuals tracking short-term environmental variability less effectively than individual
learners because the social learners’ behaviour is correlated with that of previous gener-
ations. However, the results of many field and laboratory studies suggest that the value of
social learning is usually transient. Animals may use social information for a certain time
to improve their behaviour but transfer to the next generation may be constrained
(Lefebvre and Giraldeau 1996). The ‘‘short term’’ benefit of social learning may therefore
allow individuals to track environmental variation, such as fish learning about local
predation risk from conspecifics (Brown and Laland 2003), while limiting the costs of trial
and errors. Natural selection should therefore play on individual learning, social learning,
and innate behavioural responses to optimize the behaviour depending on environmental
conditions (Boyd and Richerson 1985, 1988). When the environment changes slowly,
behaviour is likely to be dominated mainly by innate behavioural responses. When the
environment changes rapidly—but not too rapidly (Dukas 1998b)—then individual
learning may be favoured. At intermediate levels of changes social learning should be
favoured. However, this formulation lacks the additional benefits of interaction among the
different plasticity forms. Individual learning may be facilitated by innate behavioural
response and provides additional flexibility to the behaviour. Social learning may also
interact with individual learning (Galef and Whiskin 2001) by introducing new behavioural
repertoires on which individual learning may act.

Conclusions and prospects

Behavioural plasticity arises from biological evolution, individual learning, and cultural
transmission. The long debate over a clear separation between behaviour as either innate or
learned [and over the terminology used (Bateson and Mameli 2007)] has obscured the
importance of the interaction of these processes. Learning ability and innate behavioural
response share similar sensory and neural structures. Innate behavioural response evolution
increases attention to certain cues, facilitates some motor patterns, and produces some
association between cue and response. Learning ability evolution provides additional
flexibility dependent on animal experience. Thus, changes in innate behavioural responses
may accumulate over generations in reaction to long-term trends in the environment, and
then behaviour can be fine tuned by learning within the life of an individual. Learning and
innate behavioural responses share some fitness related costs, but also have some specific
ones that might be favoured under different environmental conditions. If both have been
extensively studied separately, relatively few experimental or field studies have investi-
gated the influence of one on the other in the development and evolution of animal
behaviour despite an increasing number of theoretical approaches. Recent research high-
lights how innate behavioural responses, when combined with learning, can facilitate rapid
responses to the environment (Riffell et al. 2008; Nelson 2000; Odling-Smee and
Braithwaite 2003). Little has been done to examine the interaction between learning and
innate behavioural responses. The two may be so intertwined, though, that comparisons of
behavioural plasticity among natural populations may not help to disentangle the two.
Thus, laboratory-based experiments with model organisms may be the most appropriate
starting point (e.g. Mery and Kawecki 2004a). Experimental evolution in the wild could be
a powerful approach as well (Reznick and Ghalambor 2005), particularly if longitudinal
responses to selection can be monitored. The most pressing question is whether the

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interaction of learning and innate behavioural responses results in behavioural plasticity

that is different from the sum of the parts. Field or laboratory experiments examining
ecological factors affecting the evolution of learning and innate behavioural response are
still lacking despite some growing interest (Mery and Kawecki 2005; Smid et al. 2007;
Snell-Rood and Papaj 2009; Sol et al. 2005) and may provide information concerning their
respective costs and constraints. Research on the costs of plasticity is still only beginning,
but is of great importance for addressing not only questions regarding the evolution of
behaviour but also of any other phenotypic traits. In particular, the relationships between
the costs of learning and costs of innate behavioural response have not been investigated.
Such research may require more effort in terms of large scale comparative studies and
increased knowledge on the genetic bases of behavioural plasticity.

Acknowledgments We thank N. Kohn and C. Reaume for useful comments on the manuscript. The work
was supported by an ATIP Grant from the Life Sciences Division of the Centre National de la Recherche
Scientifique and from the European Research Council under the European Community’s Seventh Frame-
work Programme (FP7/2007–2013)/ERC Grant agreement no 209540.

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