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Environmental heterogeneity and the evolution of personality traits in blue tits (Cyaniste caeruleus)
Abstract
Environmental heterogeneity, spatial variation in selection pressure and gene flow are known to be important for shaping intra-specific variation and local adaptations. However, their roles as drivers of variation and divergence in behavioral traits have seldom been studied. Here, we studied the phenotypic divergence of breeding and fledgling blue tits (Cyanistes caeruleus) for personality traits across three wild populations situated in contrasted habitats yet connected by gene flow. We first compared the mean personality phenotype of each population. Second, using common garden, reciprocal transplant and cross-fostering experiment we investigated the genetic basis of the observed divergence. Third, we determined the selection pressure acting on the personality phenotype in each population. We found phenotypic and genetic difference between populations and our results suggested that these divergences result from the local selection regime in each habitat. Overall, our results highlight the importance of environmental heterogeneity in the maintenance of small-scale intra-specific variation for behavioral traits.
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Many behavioural traits show important inter-individual phenotypic and genetic variation despite strong potential selection that should reduce this variability. Spatial and temporal heterogeneity in environmental conditions has been proposed to maintain such variation but empirical evidences supporting this hypothesis are still scarce for behavioural traits. Here, we analysed the repeatability and the ecological and individual factors that influence the expression of docility across different environmental contexts in wild eastern chipmunks (Tamias striatus) studied over a period of 10 years. We also estimated the heritability of docility and the patterns of viability selection acting on this trait for adults and juveniles. Docility was moderately repeatable among various contexts and was positively affected by age, was higher in males than that in females, was higher during the fall and decreased with population density. Heritability of docility was low at 0.17. We found disruptive selection for the survival of adults only, individuals more or less docile than average having a higher survival. Our study confirms that docility is both phenotypically and genetically variables and that disruptive selection might maintain the variability in this trait.
Significance statement
Documenting the factors allowing the maintenance of phenotypic and genetic variation of behavioural traits within natural populations is a central objective in ecology and evolution. Here, we studied a wild eastern chipmunk population over 10 years and recorded docility, a personality trait, on both juveniles and adults. We showed that docility was repeatable and that it was also heritable and influenced by different individual and environmental factors. Importantly, we also found that disruptive viability selection was acting on adult docility independently of environmental variations. Our results show that docility is both phenotypically and genetically variable and that patterns of selection acting on this trait can maintain personality heterogeneity across temporally varying environmental conditions in the wild.
Many animals show complex behaviours that can have important ecological and evolutionary consequences. Environmental variation can lead to divergent selection that consistently favours particular behaviours in different environments; but how predictably multiple aspects of animal behaviour diverge in response to different environmental conditions remains unclear. We tested whether populations evolving under different levels of predation risk show predictable and repeatable population-level behavioural differences in all five primary components of animal personality: aggression, sociability, boldness, activity and exploration. We formulated and tested a priori predictions of divergence for each behaviour using the adaptive radiation of Bahamas mosquitofish, Gambusia hubbsi (family Poeciliidae), inhabiting vertical water-filled caves (blue holes) where they have evolved for thousands of years in either the presence or absence of predatory fish. Mosquitofish behaviours differed consistently, and largely predictably, between predation regimes: low-predation mosquitofish showed reduced sociability and greater exploration of a novel environment compared to high-predation counterparts. However, some differences were sex dependent: only females showed greater boldness and only males displayed reduced aggressiveness in low-predation populations. Activity levels did not differ between predation regimes. All populations showed a behavioural syndrome characteristic of either proactive or reactive stress-coping styles with regard to exploration. Exploration behavioural syndromes were more similar among populations that evolved in similar predation regimes, regardless of genetic relatedness. Using laboratory-born, high-predation mosquitofish, we confirmed that exploratory behaviours have a genetic basis and show significant within-individual repeatability. Our results suggest that environmental variation, such as chronic predation risk, can lead to repeatable, and often predictable, changes in multifarious animal behaviours, and that various aspects of behaviour can diversify more or less independently of one another. Considering the ecological importance of these behaviours, the ability to forecast behavioural shifts in a rapidly changing world could serve as a valuable conservation tool.
Males of socially monogamous species can increase their siring success via within-pair and extra-pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five-year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as "interactive phenotypes" arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra-pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra-pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multi-level structure of male fertilization routes when studying the evolution of male mating strategies. This article is protected by copyright. All rights reserved.
Natural enemies such as predators and parasites are known to shape intra-specific variability of behaviour and personality in natural populations, yet several key questions remain: (1) What is the relative importance of predation versus parasitism in shaping intra-specific variation of behaviour across generations? (2) What are the contributions of genetic and plastic effects to this behavioural divergence? And (3) to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (1) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites, for (2) both wild-caught F0 and laboratory-reared F2 individuals and coming from (3) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory-reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild-caught F0 individuals. Third, the two lineages showed a mixture of parallel and non-parallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay-offs in alternative predation/parasitism environments, and that parasitism have more transient effects in shaping intra-specific variation of behaviour than does predation. This article is protected by copyright. All rights reserved.
Predator–prey interactions are important drivers in structuring ecological communities. However, despite widespread acknowledgement that individual behaviours and predator species regulate ecological processes, studies have yet to incorporate individual behavioural variations in a multipredator system. We quantified a prevalent predator avoidance behaviour to examine the simultaneous roles of prey personality and predator hunting mode in governing predator–prey interactions. Mud crabs, Panopeus herbstii, reduce their activity levels and increase their refuge use in the presence of predator cues. We measured mud crab mortality and consistent individual variations in the strength of this predator avoidance behaviour in the presence of predatory blue crabs, Callinectes sapidus, and toadfish, Opsanus tau. We found that prey personality and predator species significantly interacted to affect mortality with blue crabs primarily consuming bold mud crabs and toadfish preferentially selecting shy crabs. Additionally, the strength of the predator avoidance behaviour depended upon the predation risk from the predator species. Consequently, the personality composition of populations and predator hunting mode may be valuable predictors of both direct and indirect predator–prey interaction strength. These findings support theories postulating mechanisms for maintaining intraspecies diversity and have broad implications for community dynamics.
Heritable personality variation is subject to fluctuating selection in many animal taxa; a major unresolved question is why this is the case. A parsimonious explanation must involve a general ecological process: a likely candidate is the omnipresent spatiotemporal variation in conspecific density. We tested whether spatiotemporal variation in density within and among nest box plots of great tits (Parus major) predicted variation in selection acting on exploratory behaviour (n = 48 episodes of selection). We found viability selection favouring faster explorers under lower densities but slower explorers under higher densities. Temporal variation in local density represented the primary factor explaining personality-related variation in viability selection. Importantly, birds did not anticipate changes in selection by means of adaptive density-dependent plasticity. This study thereby provides an unprecedented example of the key importance of the interplay between fluctuating selection and lack of adaptive behavioural plasticity in maintaining animal personality variation in the wild.
Personality traits have recently been shown to impact fitness in different animal species, potentially making them similarly relevant drivers as morphological and life history traits along the evolutionary pathways of organisms. Predation is a major force of natural selection through its deterministic effects on individual survival, but how predation pressure has helped to shape personality trait selection, especially in free-ranging animals, remains poorly understood. We used high-precision GPS tracking to follow whole flocks of homing pigeons (Columba livia) with known personalities and morphology during homing flights where they were severely predated by raptors. This allowed us to determine how the personality and morphology traits of pigeons may affect their risk of being predated by raptors. Our survival model showed that individual pigeons, which were more tolerant to human approach, slower to escape from a confined environment, more resistant to human handling, with larger tarsi, and with lighter plumage, were more likely to be predated by raptors. We provide rare empirical evidence that the personality of prey influences their risk of being predated under free-ranging circumstances.
Behaviors are highly plastic and one aspect of this plasticity is behavioral changes over age. The presence of age-related plasticity in behavior opens up the possibility of between-individual variation in age-related plasticity (Individual-Age interaction, IxA) and genotype-age interaction (GxA). We outline the available approaches for quantifying GxA. We underline that knowledge of GxA for behaviors is an important step in reaching and understanding of the evolution of plasticity in behavior over lifetime. In particular, the heritability (repeatability) and/or the rank order of behavior across individuals are predicted to change across ages in presence of GxA. We draw on the theory of reaction norms to illustrate that GxA, when present, is likely to lead to developmental changes in the magnitude and possibly sign of the genetic correlation between behaviors (behavioral syndrome). We present an overview of the literature on changes in the ranking of individuals’ behavior across ages, and in the correlation between behaviors. Although all studies were carried out on the phenotypic level, they overall suggest clear scope for increased study of GxA as a process explaining age-related plasticity in behaviors. Lastly, we throughout emphasize that many of the approaches and underlying theory of GxA is applicable to the study of IxA, which is informative as it presents the upper limit of GxA, but is also a more attainable target of study in many systems. Empirical work aimed at understanding IxA and GxA in behavior is needed in order to understand whether patterns predicted by theory on plasticity indeed occur for age-related plasticity of behavior.
Describing and quantifying animal personality is now an integral part of behavioural studies because individually distinctive behaviours have ecological and evolutionary consequences. Yet, to fully understand how personality traits may respond to selection, one must understand the underlying heritability and genetic correlations between traits. Previous studies have reported a moderate degree of heritability of personality traits but few of these studies have either been conducted in the wild or estimated the genetic correlations between personality traits. Estimating the additive genetic variance and covariance in the wild is crucial to understand the evolutionary potential of behavioural traits. Enhanced environmental variation could reduce heritability and genetic correlations thus leading to different evolutionary predictions. We estimated the additive genetic variance and covariance of docility in the trap, sociability (mirror image stimulation), and exploration and activity in two different contexts (open-field and mirror image simulation experiments) in a wild population of yellow-bellied marmots (Marmota flaviventris). We estimated both heritability of behaviours and of personality traits and found non-zero additive genetic variance in these traits. We also found non-zero maternal, permanent environment, and year effects. Finally, we found four phenotypic correlations between traits, and one positive genetic correlation between activity in the open-field test and sociability. We also found permanent environment correlations between activity in both tests and docility and exploration in the MIS test. This is one of a handful of studies to adopt a quantitative genetic approach to explain variation in personality traits in the wild, and thus, provides important insights into the potential variance available for selection. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Variation in early nutrition is known to play an important role in shaping the behavioural development of individuals. Parental prey selection may have long-lasting behavioural influences. In birds foraging on arthropods, for instance, the specific prey types, e.g. spiders and caterpillars, matter as they have different levels of taurine which may have an effect on personality development. Here we investigated how naturally occurring variation in the amounts of spiders and caterpillars, provisioned to nestlings at day 4 and 8 after hatching, is related to the response to handling stress in a wild passerine, the great tit (Parus major). Broods were cross-fostered in a split-brood design allowing us to separate maternal and genetic effects from early rearing effects. Adult provisioning behaviour was monitored on day four and day eight after hatching using video recordings. Individual nestlings were subjected to a handling stress test at an age of 14 days, which is a validated proxy for exploratory behaviour as an adult.
Variation in handling stress was mainly determined by the rearing environment. We show that, contrary to our predictions, not the amount of spider biomass, but the amount of caterpillar biomass delivered per nestling significantly affected individual performance in the stress test. Chicks provisioned with lower amounts of caterpillars exhibited a stronger stress response, reflecting faster exploratory behaviour later on in life, than individuals who received larger amounts of caterpillars.
These results suggest that natural variation in parental behaviour in wild birds modulates the developmental trajectories of their offspring's personality via food provisioning. Since parental provisioning behaviour might also reflect the local environmental conditions, provisioning behaviour may influence how nestlings respond to these local environmental conditions.
In animal populations, as in humans, behavioural differences between individuals that are consistent over time and across contexts are considered to reflect personality, and suites of correlated behaviours expressed by individuals are known as behavioural syndromes. Lifelong stability of behavioural syndromes is often assumed, either implicitly or explicitly. Here, we use a quantitative genetic approach to study the developmental stability of a behavioural syndrome in a wild population of blue tits. We find that a behavioural syndrome formed by a strong genetic correlation of two personality traits in nestlings disappears in adults, and we demonstrate that genotype-age interaction is the likely mechanism underlying this change during development. A behavioural syndrome may hence change during organismal development, even when personality traits seem to be strongly physiologically or functionally linked in one age group. We outline how such developmental plasticity has important ramifications for understanding the mechanistic basis as well as the evolutionary consequences of behavioural syndromes.
© 2015 The Author(s) Published by the Royal Society. All rights reserved.
While the study of the origins of biological diversity across species has provided numerous examples of adaptive divergence, the realization that it can occur at microgeographic scales despite gene flow is recent, and scarcely illustrated. We review here evidence suggesting that the striking phenotypic differentiation in ecologically relevant traits exhibited by blue tits Cyanistes caeruleus in their southern range-edge putatively reflects adaptation to the heterogeneity of the Mediterranean habitats. We first summarize the phenotypic divergence for a series of life history, morphological, behavioural, acoustic and colour ornament traits in blue tit populations of evergreen and deciduous forests. For each divergent trait, we review the evidence obtained from common garden experiments regarding a possible genetic origin of the observed phenotypic differentiation as well as evidence for heterogeneous selection. Second, we argue that most phenotypically differentiated traits display heritable variation, a fundamental requirement for evolution to occur. Third, we discuss non-random dispersal, selective barriers and assortative mating as processes that could reinforce local adaptation. Finally, we show how population genomics supports isolation by environment across landscapes. Overall, the combination of approaches converge to the conclusion that the strong phenotypic differentiation observed in Mediterranean blue tits is a fascinating case of local adaptation.This article is protected by copyright. All rights reserved.
The pace-of-life syndrome (POLS) hypothesis for animal personality proposes that variation among individuals in life-history strategies is associated with consistent differences in behavior. We tested predictions of this hypothesis in the superb fairy-wren, Malurus cyaneus, by investigating long-term individual differences in risk-related behaviors (latency to enter a novel artificial environment, exploration, activity and response to mirror image stimulation) and survival. We found consistent differences between individuals in these behaviors (adjusted repeatability of exploration of artificial novel environment = 0.37). Individual differences were consistent over several years and bi-variate analyses showed a significant among-individual correlation (‘behavioral syndrome’) between exploration behavior at two life stages (young adult and old adult). Docility at the nestling stage predicted exploration behavior of juveniles. Behavioral traits measured in a risky context were correlated with one another, forming a behavioral syndrome of coping strategies ranging from ‘proactive’ to ‘reactive’. Nestlings that were more active and exploratory in isolation were less docile during handling, while adults that entered the artificial environment fast were more exploratory, active, and aggressive in the artificial environment. Exploration behavior increased within individuals as they aged and when they were in poorer condition, consistent with expectations of more risk-prone behavior with lower residual reproductive value (reduced ‘asset protection’). Risk-related behavior predicted the probability of apparent survival: more exploratory individuals were less likely to be present in the population twelve months later. Our findings suggest that, consistent with the predictions of the POLS hypothesis, individual variation in survival is associated with consistent individual differences in risk-related behavior that are maintained long-term and span developmental boundaries.
Temperament traits are seen in many animal species, and recent evolutionary models predict that they could be maintained by heterogeneous selection. We tested this prediction by examining density-dependent selection in juvenile common lizards Zootoca vivipara scored for activity, boldness and sociability at birth and at the age of one year. We measured three key life history traits (juvenile survival, body growth rate, and reproduction) and quantified selection in experimental populations at five density levels ranging from low to high values. We observed consistent individual differences for all behaviours on the short term, but only for activity and one boldness measure across the first year of life. At low density, growth selection favoured more sociable lizards, while viability selection favoured less active individuals. A significant negative correlational selection on activity and boldness existed for body growth rate irrespective of density. Thus, behavioural traits were characterised by limited ontogenic consistency and natural selection was heterogeneous between density treatments and fitness traits. This confirms that density-dependent selection plays an important role in the maintenance of individual differences in exploration-activity and sociability. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Different behavioral traits often covary, forming a behavioral syndrome. It is poorly known whether this covariance occurs on the between-individual level and what its selective consequences are. We used repeated measures (N = 562 observation events) of individual tawny owl Strix aluco females (N = 237) to study the integrated effects of seasonal timing of reproduction and clutch size on boldness displayed during defense of their clutch, in relation to plumage coloration, including local recruit production as a selective force on these traits. Using a Bayesian multivariate mixed model, we quantified the covariances between these traits on phenotypic, residual, and between-individual level and used a structural equation modeling approach to test the significance of presumed causal relationship between these traits in an a priori hypothesized path. On the phenotypic level, boldness was determined through early timing of breeding and larger clutch size, and early breeding increased recruitment probability. However, this relationship was entirely due to residual covariances and was not present on the between-individual level. The low individual-level correlations did not constrain the capacity of the population to respond to evolution as quantified by average autonomy (a metric summarizing evolutionary constraint on multiple traits). In the tawny owl, the association between early breeding and bold behavior, which is favored by selection, is solely due to extrinsic, nonheritable factors. We conclude that phenotypic evidence is insufficient to demonstrate syndrome covariance.
According to the Bpace-of-life syndrome^ concept, slow-fast life-history strategies favored under different ecological conditions should lead to co-adaptations between metabolic rate and personality traits such as activity, exploration, and boldness. Although the relationships between resting metabolic rate (RMR) and personality traits have been recently tested several times, we still do not know whether personality is related to the daily energy expenditure (DEE) of free-living individuals in their natural habitat. The objectives of this study were to assess the links between RMR, DEE, and two personality traits (exploration in an open-field and docility during handling) in wild eastern chipmunks (Tamias striatus). Using a multivariate mixed model, we found that exploration and docility were significantly correlated at the among-individual level, confirming the presence of a behavioral syndrome within our population. We also found that exploration, but not docility, was negatively correlated with DEE. Hence, fast explorers show lower DEE levels than slow explorers, independently of RMR and docility. This result adds to an increasingly large (and complex) literature reporting the impacts of personality traits on the biology, ecology, and physiology of animals in their natural environment.
Capsule The blue colour of the coverts and crowns of Blue Tits Cyanistes caeruleus and Great Tits Parus major is influenced by sex, age and environmental factors. Aims To quantify the blueness of two species of tits breeding in different habitats in Britain. Methods By manipulating daylength in the laboratory, adult Blue Tits were induced to moult at fast and slow speeds. When they had finished, the blue colour of their wing coverts and crowns was measured (in the range visible to human observers), and compared with the colour of birds caught in the field. Results As well as highly significant sex and age differences in colour, Blue Tits were 26% bluer in 1998 than 2000, and male Great Tits were 15% less blue in small woods than in large woods in our study population in East Anglia, England. Both species became more saturated with blue up to the age of three years. British Cy. c. obscurus were darker blue than Cy. c. caeruleus of Continental Europe Conclusions There are significant environmental influences on the blueness of British tits in addition to the well-known age and sex effects.
The interactions between organisms and their environments can shape distributions of spatial genetic variation, resulting in patterns of isolation by environment (IBE) in which genetic and environmental distances are positively correlated, independent of geographic distance. IBE represents one of the most important patterns that results from the ways in which landscape heterogeneity influences gene flow and population connectivity, but it has only recently been examined in studies of ecological and landscape genetics. Nevertheless, the study of IBE presents valuable opportunities to investigate how spatial heterogeneity in ecological processes, agents of selection, and environmental variables contributes to genetic divergence in nature. New and increasingly sophisticated studies of IBE in natural systems are poised to make significant contributions to our understanding of the role of ecology in genetic divergence and of modes of differentiation both within and between species. Here, we describe the underlying ecological processes that can generate patterns of IBE, examine its implications for a wide variety of disciplines, and outline several areas of future research that can answer pressing questions about the ecological basis of genetic diversity.This article is protected by copyright. All rights reserved.
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Recent publications on animal conservation called out the need to account for individual and among-population differences in dispersal. Despite the demonstrated links between personality traits and dispersal behavior, most studies of local adaptation have focused on dispersal capacity through variation in morphology and physiology. Ephemeral habitat patches generally favor dispersal capacity, whereas loss and increasing isolation of the patches can select against dispersal capacity. In this study, we explore whether populations of Natterjack toads (Bufo calamita) have evolved different morphologies, physiological performance and personality traits in response to the spatial arrangement of their habitat. First, we studied the consistency and intercorrelations of behavioral traits in order to test for the possible existence of personality, which so far has been largely ignored in the study of amphibians. Second, we assessed levels of population differentiation in candidate personality traits and dispersal capacity. The toadlets in this study originated from populations with different degrees of isolation, due to distance from other populations and resistance of the surrounding landscape, and with different dynamics of the subpopulations. We used two cohorts of toadlets, one raised in a common environment and the other collected in the field. We found consistency and correlations between the behavioral mea-surements, suggesting the possible existence of personality linked to mobility. The higher locomotor performance in toadlets from the metapopulations in the low-resistance landscape compared with those from the isolated populations indicates local adaptation in dispersal capacity. Yet, we could not demonstrate that differences in behavior can be explained by local adaptation in dispersal-related traits.
Populations of guppies, Poecilia reticulata and Hart's rivulus, Rivulus harti, in Trinidad experience different levels of predation hazard from piscivorous fish. Those from the larger rivers (downstream sites) experience chronically high predation hazard, while those from headwater streams (upstream sites) have few predators. Guppies and Hart's rivulus, collected from downstream and upstream sites, were assayed for their feeding rate in the presence and absence of predators. We defined tenacity as the ratio of the feeding rates in the presence and absence of a predator stimulus. Thus, tenacity expresses the degree to which the forager maintains its feeding rate when a predator stimulus is present. Previous work by Seghers (1973) showed that non-feeding guppies from downstream sites responded more strongly to predators than did guppies from upstream sites. Based on this, we initially hypothesized that fish from downstream sites would show lower tenacities than fish from upstream sites. However, we found the opposite in every case. When confronted with a predator stimulus, guppies and Hart's rivulus from downstream sites fed at consistently greater rates and displayed greater tenacities than did those from upstream sites. These differences were found in experiments using both live and model predators. The results suggest that upstream fish readily trade off feeding for hiding and avoiding predation hazard, a likely response when predators appear infrequently, while downstream fish appear to be selected for boldness and tenacity while foraging under chronically high hazard.
Maximum likelihood or restricted maximum likelihood (REML) estimates of the
parameters in linear mixed-effects models can be determined using the lmer
function in the lme4 package for R. As for most model-fitting functions in R,
the model is described in an lmer call by a formula, in this case including
both fixed- and random-effects terms. The formula and data together determine a
numerical representation of the model from which the profiled deviance or the
profiled REML criterion can be evaluated as a function of some of the model
parameters. The appropriate criterion is optimized, using one of the
constrained optimization functions in R, to provide the parameter estimates. We
describe the structure of the model, the steps in evaluating the profiled
deviance or REML criterion, and the structure of classes or types that
represents such a model. Sufficient detail is included to allow specialization
of these structures by users who wish to write functions to fit specialized
linear mixed models, such as models incorporating pedigrees or smoothing
splines, that are not easily expressible in the formula language used by lmer.
Offspring provisioning and nest defence are important forms of parental care. In birds, parents that engage in nest defence behaviour have to interrupt nestling provisioning with potentially harmful consequences for offspring growth and condition. To maximize fitness, parents should trade off optimal levels of offspring provisioning versus nest defence, but relatively little is known about how parents allocate their time between these two activities and how parental decisions to postpone provisioning vary as a function of the intensity of nest predation risk. We found that pairs of blue tits, Cyanistes caeruleus, adjusted parental care behaviours according to perceived immediate risk levels by switching from offspring provisioning to nest defence. In the presence of a direct nest predation threat, parents interrupted offspring provisioning for longer than in response to a novel object close to the nest, but still gradually resumed provisioning activity, probably because of a decrease in perceived predation risk over time. By increasing their provisioning effort once the immediate threat had diminished, parents compensated at least partly for the lost provisioning opportunities during high-risk situations. Hence, by adaptively adjusting the temporal trade-off between different parental care behaviours according to the perceived risk, blue tits are presumably able to mitigate potential negative long-term consequences of interruptions in provisioning during high-risk situations for offspring growth and condition.
Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy-bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether 'exploration behaviour', a captive assay of the shy-bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.
Organisms use environmental cues to time their life-cycles and among these cues, photoperiod is the main trigger of reproductive behaviours such as territory defence or song activity. Whether photoperiod is also important for another behaviour closely associated with reproduction, mate choice, is unknown. In many bird species, mate choice occurs at two different times during the annual cycle that strongly differ in daylength: in late winter when photoperiod is short and social mates are chosen, and again around egg-laying when photoperiod is longer and extra-pair mates are chosen. This duality makes the role that photoperiod plays on mate choice behaviours intriguing. We investigated the effect of photoperiod on mate choice using three experimental photoperiodic treatments (9 L:15 D, 14 L:10 D, 18 L:6 D), using blue tits (Cyanistes caeruleus) as a biological model. We show that female choice was stronger under long photoperiods. In addition, female blue tits spent significantly more time near males with long tarsi and long wings. This latter preference was only expressed under long photoperiods, suggesting that some indices of male quality only become significant to females when they are strongly photostimulated, and therefore that females could select their social and extra-pair mates based on different phenotypic traits. These results shed light on the roles that photoperiod may play in stimulating pair-bonding and in refining female selectivity for male traits.
Behavioral differences between individuals that are consistent over time characterize animal personality. The existence of such consistency contrasts to the expectation based on classical behavioral theory that facultative behavior maximizes individual fitness. Here, we study two personality traits (aggression and breath rate during handling) in a wild population of blue tits during 2007-2012. Handling aggression and breath rate were moderately heritable (h (2) = 0.35 and 0.20, respectively) and not genetically correlated (r A = 0.06) in adult blue tits, which permits them to evolve independently. Reciprocal cross-fostering (2007-2010) showed that offspring reared by more aggressive males have a higher probability to recruit. In addition, offspring reared by pairs mated assortatively for handling aggression had a higher recruitment probability, which is the first evidence that both parents' personalities influence their reproductive success in the wild in a manner independent of their genetic effects. Handling aggression was not subjected to survival selection in either sex, but slow-breathing females had a higher annual probability of survival as revealed by capture-mark-recapture analysis. We find no evidence for temporal fluctuations in selection, and thus conclude that directional selection (via different fitness components) acts on these two heritable personality traits. Our findings show that blue tit personality has predictable fitness consequences, but that facultative adjustment of an individual's personality to match the fitness maximum is likely constrained by the genetic architecture of personality. In the face of directional selection, the presence of heritable variation in personality suggests the existence of a trade-off that we have not identified yet.
In a rapidly changing world, it is of fundamental importance to understand processes constraining or facilitating adaptation through microevolution. As different traits of an organism covary, genetic correlations are expected to affect evolutionary trajectories. However, only limited empirical data are available.
We investigate the extent to which multivariate constraints affect the rate of adaptation, focusing on four morphological traits often shown to harbour large amounts of genetic variance and considered to be subject to limited evolutionary constraints. Our data set includes unique long-term data for seven bird species and a total of 10 populations. We estimate population-specific matrices of genetic correlations and multivariate selection coefficients to predict evolutionary responses to selection. Using Bayesian methods that facilitate the propagation of errors in estimates, we compare (1) the rate of adaptation based on predicted response to selection when including genetic correlations with predictions from models where these genetic correlations were set to zero and (2) the multivariate evolvability in the direction of current selection to the average evolvability in random directions of the phenotypic space. We show that genetic correlations on average decrease the predicted rate of adaptation by 28%. Multivariate evolvability in the direction of current selection was systematically lower than average evolvability in random directions of space. These significant reductions in the rate of adaptation and reduced evolvability were due to a general nonalignment of selection and genetic variance, notably orthogonality of directional selection with the size axis along which most (60%) of the genetic variance is found.
These results suggest that genetic correlations can impose significant constraints on the evolution of avian morphology in wild populations. This could have important impacts on evolutionary dynamics and hence population persistence in the face of rapid environmental change.
Local adaptation has been a major focus of evolutionary ecologists working across diverse systems for decades. However, little of this research has explored variation at microgeographic scales because it has often been assumed that high rates of gene flow will prevent adaptive divergence at fine spatial scales. Here, we establish a quantitative definition of microgeographic adaptation based on Wright's dispersal neighborhood that standardizes dispersal abilities, enabling this measure to be compared across species. We use this definition to evaluate growing evidence of evolutionary divergence at fine spatial scales. We identify the main mechanisms known to facilitate this adaptation and highlight illustrative examples of microgeographic evolution in nature. Collectively, this evidence requires that we revisit our understanding of the spatial scale of adaptation and consider how microgeographic adaptation and its driving mechanisms can fundamentally alter ecological and evolutionary dynamics in nature.
The direction of covariation in behavioral traits (a behavioral syndrome) is typically the same in males and females, although intersexual
differences in life history could lead to intersexual heterogeneity in syndrome structure. We explored whether a behavioral
syndrome was the same in both sexes. We recorded 2 metrics of nest defense in wild blue tits Cyanistes caeruleus: 1) Nest defense of
a female around the time her eggs hatch (hatching defense), 2) nest defense of the male and female parent when their offspring was
16 days old (nestling defense), and 3) handling aggression. We used repeated records of these behaviors collected on 392 females and
363 males during 2007–2012 in a hierarchical mixed model to separate the between-individual from the residual (co)variances. We find
that 1) hatching defense is not repeatable across breeding seasons (but highly repeatable within years). 2) Nestling defense intensity is
38% repeatable in males and females. 3) Contrary to our expectation, females that defended their nestlings more intensively were less
aggressive when being handled (negative between-individual correlation), but 4) nestling defense and handling aggression showed a
positive between-individual correlation in males although nonsignificantly. These correlations were completely masked on the phenotypic
level by a low residual correlation. Individuals may hence display repeatable and correlated aggressive behavior in different contexts,
but the direction of this syndrome may differ between the sexes. Intersexual heterogeneity in animal personality and syndrome
structure remains poorly understood, and our findings hence urge future work to explicitly consider this heterogeneity.
Environmental heterogeneity can result in spatial variation in selection pressures that can produce local adaptations. The pace-of-life syndrome hypothesis predicts that habitat-specific selective pressures will favor the coevolution of personality, physiological, and lifehistory phenotypes. Few studies so far have compared these traits simultaneously across different ecological conditions. In this study, we compared 3 personality traits (handling aggression, exploration speed in a novel environment, and nest defense behavior) and 1 physiological trait (heart rate during manual restraint) across 3 Corsican blue tit (Cyanistes caeruleus) populations. These populations are located in contrasting habitats (evergreen vs. deciduous) and are situated in 2 different valleys 25 km apart. Birds from these populations are known to differ in life-history characteristics, with birds from the evergreen habitat displaying a slow pace-of-life, and birds from the deciduous habitat a comparatively faster pace-of-life. We expected personality to differ across populations, in line with the differences in pace-of-life documented for life-history traits. As expected, we found behavioral differences among populations. Despite considerable temporal variation, birds exhibited lower handling aggression in the evergreen populations. Exploration speed and male heart rate also differed across populations, although our results for exploration speed were more consistent with a phenotypic difference between the 2 valleys than between habitats. There were no clear differences in nest defense intensity among populations. Our study emphasizes the role of environmental heterogeneity in shaping population divergence in personality traits at a small spatial scale.
The use of regression techniques for estimating the direction and magnitude of selection from measurements on phenotypes has become widespread in field studies. A potential problem with these techniques is that environmental correlations between fitness and the traits examined may produce biased estimates of selection gradients. This report demonstrates that the phenotypic covariance between fitness and a trait, used as an estimate of the selection differential in estimating selection gradients, has two components: a component induced by selection itself and a component due to the effect of environmental factors on fitness. The second component is shown to be responsible for biases in estimates of selection gradients. The use of regressions involving genotypic and breeding values instead of phenotypic values can yield estimates of selection gradients that are not biased by environmental covariances. Statistical methods for estimating the coefficients of such regressions, and for testing for biases in regressions involving phenotypic values, are described.
We tested the two main evolutionary hypotheses for an association between immunity and personality. The risk-of-parasitism hypothesis predicts that more proactive (bold, exploratory, risk-taking) individuals have more vigorous immune defenses because of increased risk of parasite exposure. In contrast, the pace-of-life hypothesis argues that proactive behavioral styles are associated with shorter lifespans and reduced investment in immune function. Mechanistically, associations between immunity and personality can arise because personality differences are often associated with differences in condition and stress responsiveness, both of which are intricately linked with immunity. Here we investigate the association between personality (measured as proactive exploration of a novel environment) and three indices of innate immune function (the non-specific first line of defense against parasites) in wild superb fairy-wrens Malurus cyaneus. We also quantified body condition, hemoparasites (none detected), chronic stress (heterophil:lymphocyte ratio) and circulating corticosterone levels at the end of the behavioral test (CORT, in a subset of birds). We found that fast explorers had lower titers of natural antibodies. This result is consistent with the pace-of-life hypothesis, and with the previously documented higher mortality of fast explorers in this species. There was no interactive effect of exploration score and duration in captivity on immune indices. This suggests that personality-related differences in stress responsiveness did not underlie differences in immunity, even though behavioral style did modulate the effect of captivity on CORT. Taken together these results suggest reduced constitutive investment in innate immune function in more proactive individuals.
Predators can affect prey both directly (consumptive effects) and indirectly (nonconsumptive effects), with a growing body
of literature showing the latter may have pronounced effects. Prey populations are comprised of individuals that differ in
perception of and willingness to take risk; therefore, studying how different types of individuals respond to predation risk
is necessary to fully understand prey dynamics. Playbacks were used to experimentally manipulate perceived predation risk
in nest-box populations of wild great tits (Parus major) to examine the nonconsumptive effects of avian predators on prey behavior and morphology, and to explore individual differences
in prey response. Individuals responded to our treatment, and responses differed depending on both treatment and premanipulation
behavioral type. Birds in areas exposed to predator playback tended to decrease in body mass more than birds exposed to nonthreatening
(control) playback. Differences between treatment groups were mainly driven by initially fast exploring birds: In the control
treatment, fast explorers increased in mass, whereas the initially fast exploring birds in the predation treatment decreased
in mass. Furthermore, birds exposed to predator playback decreased exploratory tendency compared with controls. These findings
demonstrate that predation risk alters great tit behavior (exploration) and morphology (body mass) and that plasticity in
response to risk relates to an individual’s willingness to take risks. Our findings suggest that individuals differ in susceptibility
to predation risk, causing adaptive individual differences in responsiveness to changes in predation risk. Acknowledging individuality
in responses to perceived predation risk has important consequences for understanding prey dynamics.
This book had its origin when, about five years ago, an ecologist (MacArthur) and a taxonomist and zoogeographer (Wilson) began a dialogue about common interests in biogeography. The ideas and the language of the two specialties seemed initially so different as to cast doubt on the usefulness of the endeavor. But we had faith in the ultimate unity of population biology, and this book is the result. Now we both call ourselves biogeographers and are unable to see any real distinction between biogeography and ecology.
Linking population genetic variation to the spatial heterogeneity of the environment is of fundamental interest to evolutionary biology and ecology, in particular when phenotypic differences between populations are observed at biologically small spatial scales. Here, we applied restriction-site associated DNA sequencing (RAD-Seq) to test whether phenotypically differentiated populations of wild blue tits (Cyanistes caeruleus) breeding in a highly heterogeneous environment exhibit genetic structure related to habitat type. Using 12 106 SNPs in 197 individuals from deciduous and evergreen oak woodlands, we applied complementary population genomic analyses, which revealed that genetic variation is influenced by both geographical distance and habitat type. A fine-scale genetic differentiation supported by genome- and transcriptome-wide analyses was found within Corsica, between two adjacent habitats where blue tits exhibit marked differences in breeding time while nesting < 6 km apart. Using redundancy analysis (RDA), we show that genomic variation remains associated with habitat type when controlling for spatial and temporal effects. Finally, our results suggest that the observed patterns of genomic differentiation were not driven by a small proportion of highly differentiated loci, but rather emerged through a process such as habitat choice, which reduces gene flow between habitats across the entire genome. The pattern of genomic isolation-by-environment closely matches differentiation observed at the phenotypic level, thereby offering significant potential for future inference of phenotype-genotype associations in a heterogeneous environment.
Behavioural syndromes, i.e. correlated behaviours, may be a result from adaptive correlational selection but in a new environmental setting the trait correlation might act as an evolutionary constraint. However, knowledge about the quantitative genetic basis of behavioural syndromes, and the stability and evolvability of genetic correlations under different ecological conditions is limited. We investigated the quantitative genetic basis of correlated behaviours in the freshwater isopod Asellus aquaticus. In some Swedish lakes, A. aquaticus has recently colonised a novel habitat and diverged into two ecotypes, presumably due to habitat specific selection from predation. Using a common garden approach and animal model analyses, we estimated quantitative genetic parameters for behavioural traits, and compared the genetic architecture between the ecotypes. We report that the genetic covariance structure of the behavioural traits has been altered in the novel ecotype, demonstrating divergence in behavioural correlations. Thus, our study confirms that genetic correlations behind behaviours can change rapidly in response to novel selective environments. This article is protected by copyright. All rights reserved.
Individual differences in personality affect behavior in novel or challenging situations. Personality traits may be subject to selection because they affect the ability to dominate others. We investigated whether dominance rank at feeding tables in winter correlated with a heritable personality trait (as measured by exploratory behavior in a novel environment) in a natural population of great tits, Parus major. We provided clumped resources at feeding tables and calculated linear dominance hierarchies on the basis of observations between dyads of color-ringed individuals, and we used an experimental procedure to measure individual exploratory behavior of these birds. We show that fast-exploring territorial males had higher dominance ranks than did slow-exploring territorial males in two out of three samples, and that dominance related negatively to the distance between the site of observation and the territory. In contrast, fast-exploring nonterritorial juveniles had lower dominance ranks than did slow-exploring nonterritorial juveniles, implying that the relation between dominance and personality is context-dependent in the wild. We discuss how these patterns in dominance can explain earlier reported effects of avian personality on natal dispersal and fitness. Copyright 2004.
(1) The aim of this paper is to estimate the shape of the curve relating first year survival to nestling weight in individual great tits (Parus major) and to study the causality of this relationship. (2) Data were collected in a mainland and an island population. Nestlings were weighed and sexed in the nest when 2 weeks old. A recapture programme provided data for recapture-rate estimates in the winter. Local survival until next breeding season was estimated by capturing the breeding population. Brood-size manipulation experiments were performed in the mainland population in order to manipulate nestling weights. (3) The relation between local recapture rate and nestling weight was described using logistic regression techniques. The descriptive model included positive weight and negative squared weight regression coefficients, if controlled for year, sex and date. Recapture rate approached zero at weights of c. 70% of the adult body weight. The curves for both populations showed an approximately linear part over a rather long range of weights. At high weights, the curve levelled off in the mainland population and curved down in the island population. (4) Survival from weighing till fledging and recapture rate from fledging till winter were related to nestling weight, but recapture rate from winter till breeding was not. (5) The effect of brood-size manipulation on nestling weight and subsequent recapture rate suggests causality of the recapture rate-nestling weight curve. Additional information from a comparison of the association between recapture rate and nestling weight within and between broods leads to the conclusion that weight does play a causal role in this relationship. Recapture rate-nestling weight curves can thus be estimated from non-experimental data.
Frequency dependent selection is thought to be a major contributor to the maintenance of phenotypic variation. We tested for frequency dependent selection on contrasting behavioral strategies, termed here 'personalities', in three species of social spiders, each thought to represent an independent evolutionary origin of sociality. The evolution of sociality in the spider genus Anelosimus is consistently met with the emergence of two temporally-stable discrete personality types: an 'aggressive' or 'docile' form. We assessed how the foraging success of each phenotype changes as a function of its representation within a colony. We did this by creating experimental colonies of various compositions (6 aggressive, 3 aggressive and 3 docile, 1 aggressive and 5 docile, 6 docile), maintaining them in a common garden for three weeks, and tracking the mass gained by individuals of either phenotype. We found that both the docile and aggressive phenotype experienced their greatest mass gain in mixed colonies of mostly docile individuals. However, the performance of both phenotypes decreased as the frequency of the aggressive phenotype increased. Nearly identical patterns of phenotype-specific frequency dependence were recovered in all three species. Naturally-occurring colonies of these spiders exhibit mixtures dominated by the docile phenotype, suggesting that these spiders may have evolved mechanisms to maintain the compositions that maximize the success of the colony without compromising the expected reproductive output of either phenotype. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Extensive literature shows that lepidopteran larvae constitute the most important component of the diet of nestling tits (Parus spp.). In Blue Tits Parus caeruleus, breeding is usually timed to match the nestling stage to the period when caterpillars are most abundant. This is true even in places where caterpillars are not very numerous and many alternative prey types have to be used. In a study of a Corsican Blue Tit P. c. ogliastrae population, characterised by the extensive use of non-cater-pillar prey, we compared some aspects of the behaviour of nestlings when fed caterpillars, grasshoppers and spiders. The expectation deduced from ecological and behavioural literature that nestlings should be best able to swallow caterpillars was confirmed. Chick prey handling time could be ranked from caterpillars (the shortest time), through spiders to grasshoppers (the longest time). Handling time increased exponentially with prey size within each prey category and was to some extent subject to variation between broods. Consequently, the behaviour of nestlings provides new support for the idea that Blue Tits are best adapted to eating caterpillars and that mechanical constraints prevent them from using very big prey items, especially non-caterpillar prey, and that this is likely to affect their choice of prey. Such constraints may be less strict in Great Tits Parus major because of their larger body size.
An exciting area in behavioural ecology focuses on understanding why animals exhibit consistent among-individual differences in behaviour (animal personal-ities). Animal personality has been proposed to emerge as an adaptation to individual differences in state vari-ables, leading to the question of why individuals differ consistently in state. Recent theory emphasizes the role that positive feedbacks between state and behaviour can play in producing consistent among-individual covari-ance between state and behaviour, hence state-dependent personality. We review the role of feedbacks in recent models of adaptive personalities, and provide guidelines for empirical testing of model assumptions and predictions. We discuss the importance of the me-diating effects of ecology on these feedbacks, and pro-vide a roadmap for including state–behaviour feedbacks in behavioural ecology research. State–behaviour feedbacks and the emergence of personality differences The past decade has seen tremendous interest in animal personalities [1–3], stemming from accumulating evidence for individual repeatability and significant correlations between various behaviours (e.g., boldness, aggres-siveness, activity, exploration, or sociability). Empirical studies show that animal personalities and behavioural syndromes (correlations across contexts) vary as a function of ecology [4,5]; for example, aggressiveness and boldness are often positively correlated but the strength of this correlation varies depending on the predation regime [6,7]. Variation in syndrome structure also exists across different temporal scales; for instance, early experiences (e.g., exposure to stressors) can have large effects on the development of personality structure but such effects can
Climate change, habitat alteration, range expansions, and biological invasions are all predicted to require rapid shifts in multiple traits including behavior and life history, both for initial population establishment and subsequent adaptation. Hormonal mechanisms likely play a key role in facilitating or constraining plastic and genetic responses for suites of traits, but few studies have evaluated their role in shaping contemporary adaptation or diversification. We examined multiple phenotypic adjustments and associated hormonal changes following a recent (early 1980s) colonization event, in which a temperate-breeding songbird, the dark-eyed junco (Junco hyemalis), became established in the Mediterranean climate of San Diego, California. The milder climate has led to an extended breeding season and year-round residency, and we document shifts in multiple sexually selected behaviors and plumage traits. Testosterone titers in San Diego were elevated for longer but with a lower peak value compared to a nearby native-range population, and correlations between testosterone and related traits were similar within and among populations. A common garden study indicated that changes in testosterone likely represent plastic responses to the less seasonal environment of the city, providing the context against which subsequent genetic changes in morphology likely occurred. We argue that correlated shifts in multiple traits, organized by underlying physiology, may be a generally important element of many successful adjustments to changing environments.
Temporal variation in selection has long been proposed as a mechanism by which genetic variation could be maintained despite short-term strong directional selection and has been invoked to explain the maintenance of consistent individual differences in behaviour. We tested the hypothesis that ecological changes through time lead to fluctuating selection, which could promote the maintenance of variation in female behavioural traits in a wild population of North American red squirrels. As predicted, linear selection gradients on female aggression and activity significantly fluctuated across years depending on the level of competition among juveniles for vacant territories. This selection acted primarily through juvenile overwinter survival rather than maternal fecundity. Incorporating uncertainty in individual measures of behaviour reduced the magnitude of annual selection gradients and increased uncertainty in these estimates, but did not affect the overall pattern of temporal fluctuations in natural selection that coincided with the intensity of competition for vacant territories. These temporal fluctuations in selection might, therefore, promote the maintenance of heritable individual differences in behaviour in this wild red squirrel population.
Animals with parental care defend their offspring with an intensity reflecting parental investment. Parental investment theory predicts that parents should take risks relative to their residual reproductive value. Therefore, parental defense should change consistently with age reaching a peak at middle age, and it should vary consistently with age at start and end of reproduction. We recorded the intensity of parental defense of offspring in 410 female goshawks Accipiter gentilis throughout their lives, ranging from timid females that barely approached a human intruder at the nest to aggressive females that physically attacked the human. Females were con-sistent in their level of defense throughout life, and aggressive females were mated to aggressive males. Investment in reproduction as reflected by laying date, clutch size, and brood size showed a bell-shaped relationship with age. Females that started to breed at a young age were less aggressive than females that started late. Likewise, females that finished reproduction at a young age behaved less aggressively than females that finished at an old age. The intensity of defense of offspring peaked at an intermediate age followed by a decrease into old age and senescence. Females that started to breed early during the season were more aggressive than late breeders. These findings are consistent with the hypothesis that the intensity of parental defense of their offspring reflects parental investment and patterns of aging.
1. Here, I present a new, multifunctional phylogenetics package, phytools, for the R statistical computing environment.
2. The focus of the package is on methods for phylogenetic comparative biology; however, it also includes tools for tree inference, phylogeny input/output, plotting, manipulation and several other tasks.
3. I describe and tabulate the major methods implemented in phytools, and in addition provide some demonstration of its use in the form of two illustrative examples.
4. Finally, I conclude by briefly describing an active web-log that I use to document present and future developments for phytools. I also note other web resources for phylogenetics in the R computational environment.
Behaviors are commonly correlated between individuals in so-called behavioral syndromes. Between-individual correlations of phenotypic traits can change the trajectories of evolutionary responses available to populations and even prevent evolutionary change if underpinned by genetic correlations. Whether behavioral syndromes also influence the course of evolution in this manner remains unknown. Here, we provide the first test of the degree to which evolutionary responses might be affected by behavioral syndrome structure. This test, based on a meta-analysis of additive genetic variancecovariance matrices, shows that behavioral syndromes constrain potential evolutionary responses by an average of 33%. For comparison, correlations between life-history or between morphological traits suggest constraints of 1318%. This finding demonstrates that behavioral syndromes might substantially constrain the evolutionary trajectories available to populations, prompts novel future directions for the study of behavioral syndromes, emphasizes the importance of viewing syndrome research from an evolutionary perspective, and provides a bridge between syndrome research and theoretical quantitative genetics.