Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities

Personalities are general properties of humans and other animals. Different personality traits are phenotypically correlated, and heritabilities of personality traits have been reported in humans and various animals. In great tits, consistent heritable differences have been found in relation to exploration, which is correlated with various other personality traits. In this paper, we investigate whether or not risk-taking behaviour is part of these avian personalities. We found that (i) risk-taking behaviour is repeatable and correlated with exploratory behaviour in wild-caught hand-reared birds, (ii) in a bi-directional selection experiment on 'fast' and 'slow' early exploratory behaviour, bird lines tend to differ in risk-taking behaviour, and (iii) within-nest variation of risk-taking behaviour is smaller than between-nest variation. To show that risk-taking behaviour has a genetic component in a natural bird population, we bred great tits in the laboratory and artificially selected 'high' and 'low' risk-taking behaviour for two generations. Here, we report a realized heritability of 19.3 +/- 3.3% (s.e.m.) for risk-taking behaviour. With these results we show in several ways that risk-taking behaviour is linked to exploratory behaviour, and we therefore have evidence for the existence of avian personalities. Moreover, we prove that there is heritable variation in more than one correlated personality trait in a natural population, which demonstrates the potential for correlated evolution.     

Repeatability and heritability of exploratory behaviour in great tits from the wild

We investigated whether individual great tits, Parus major, vary consistently in their exploratory behaviour in a novel environment and measured the repeatability and heritability of this trait. Wild birds were caught in their natural habitat, tested in the laboratory in an open field test on the following morning, then released at the capture site. We measured individual consistency of exploratory behaviour for recaptured individuals (repeatability) and estimated the heritability with parent-offspring regressions and sibling analyses. Measures of exploratory behaviour of individuals at repeated captures were consistent in both sexes and study areas (repeatabilities ranged from 0.27 to 0.48). Exploration scores did not differ between the sexes, and were unrelated to age, condition at fledging or condition during measurement. Heritability estimates were 0.22-0.41 (parent-offspring regressions) and 0.37-0.40 (sibling analyses). We conclude that (1) consistent individual variation in open field behaviour exists in individuals from the wild, and (2) this behavioural variation is heritable. This is one of the first studies showing heritable variation in a behavioural trait in animals from the wild, and poses the question of how this variation is maintained under natural conditions. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Heritability of the timing of autumn migration in a natural bird population

In recent decades, global temperature has increased at an unprecedented rate. This has been causing rapid environmental shifts that have altered the selective regimes determining the annual organization of birds. In order to assess the potential for adaptive evolution in the timing of autumn migration, we estimated heritabilities of the onset of migratory activity in a southern German blackcap (Sylvia atricapilla) population. Heritabilities (h2=0.34-0.45) and coefficients of additive genetic variation (CV(A)=4.7-5.7) were significant and consistent when estimated by different methods, irrespective of whether they were derived from birds hatched in the wild or bred in captivity. In an artificial selection experiment, we selected for later onset of migratory activity, simulating expected natural selection on this trait. We obtained a significant delay in the mean onset of migratory activity by more than one week after two generations of selection. Realized heritability (h2=0.55) was in agreement with expected heritability in the cohort that the selection line was derived from. Our results suggest that evolutionary changes in the timing of autumn migration may take place over a very short time period and will most probably be unconstrained by the lack of additive genetic variation.     

(S)he who dares, grows! A cross‐population study of growth and behaviour in three‐spined sticklebacks

Three‐spined sticklebacks ( Gasterosteus aculeatus ) exhibit considerable inter‐population variation in behaviour, morphology and life history characteristics. Such population‐level variation can be generated directly by environmental characteristics of the water body they inhabit ( e.g . temperature regimes, which directly influence growth rates) but local genetic adaptation is also important. By performing 'common garden' experiments, in which laboratory‐bred individuals from separate populations are raised under standardized controlled laboratory conditions, it is possible to identify genetically‐based population‐level phenotype variation. Here we present the results of two studies, carried out using juvenile three‐spined sticklebacks bred from parental stock from five geographically isolated UK populations and reared under standard laboratory ('common garden') conditions. Firstly we report the results of a study examining population‐level variation in patterns of early growth, in which we tracked the growth of replicate groups of full‐sibs from all five populations, from hatching to 126d. Secondly we report the results of an experimental behavioural study, designed to examine population‐level variation in the exploratory or 'boldness' behaviour of laboratory‐bred and reared juvenile three‐spined sticklebacks from the same five populations. We discuss how adaptive genetically based patterns of behaviour and growth may co‐vary across populations.     

Variation in heritability of tadpole growth: an experimental analysis

Heritability characteristically shows large variation between traits, among populations and species, and through time. One of the reasons for this is its dependence on gene frequencies and how these are altered by selection and drift through the evolutionary process. We studied variation in heritability of tadpole growth rate in populations of the Swedish common frog, Rana temporaria. In populations evolving under warmer conditions, we have demonstrated elsewhere that tadpoles show better growth and physiological performance at relatively higher temperatures than tadpoles with an evolutionary history in a relatively cooler part of the distribution range. In the current study, we ask whether this process of divergence under natural selection has influenced the genetic architecture as visualised in estimates of heritability of growth rate at different temperature treatments under laboratory conditions. The results suggest that the additive genetic variance varies between treatments and is highest in a treatment that is common to both populations. Our estimates of narrow sense heritability are generally higher in the thermal regime that dominates in the natural environment. The reason for this appears not primarily to be because the component of additive genetic variation is higher in relation to the total phenotypic variation under these conditions, but because the part of the phenotypic variance explained by environmental variation increases at temperatures to which the current populations has been less frequently under selection.     

Effects of the rearing environment on average behaviour and behavioural variation in steelhead

In the context of conservation hatcheries that seek to bolster wild populations by releasing captively-reared fishes into the wild, steelhead Oncorhynchus mykiss were used to test the hypothesis that naturalistic rearing environments promote adaptive behaviour that might otherwise not develop in typical hatchery environments. When comparisons were made among fish reared in barren, structured or structurally variable environments ( i.e. the location of the structure was repositioned every 2–3 days), structure in the rearing environment increased future exploratory behaviour, but only if the structure was stable. Under conditions of high perceived predation risk, the fish no longer exhibited increased exploratory behaviour, suggesting that it is expressed in an adaptive, context-dependant manner. Another concern with hatcheries is that relaxed selection over multiple generations in captivity can increase maladaptive behavioural variation. Compared to rearing in hatchery-typical barren environments, rearing in structured-stable environments decreased behavioural variation. This effect, which occurred during development and did not involve selection, demonstrates a different mechanism for change in behavioural variation in captivity. These experiments show that effects of structure and structural stability occur at the level of both average behaviour and behavioural variation, and suggest that these effects should be considered when fishes are reared in hatcheries for later release into the wild.     

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (<Emphasis Type="Italic">Salmo trutta</Emphasis>) populations

Captive bred individuals are often released into natural environments to supplement resident populations. Captive bred salmonid fishes often exhibit lower survival rates than their wild brethren and stocking measures may have a negative influence on the overall fitness of natural populations. Stocked fish often stem from a different evolutionary lineage than the resident population and thus may be maladapted for life in the wild, but this phenomenon has also been linked to genetic changes that occur in captivity. In addition to overall loss of genetic diversity via captive breeding, adaptation to captivity has become a major concern. Altered selection pressure in captivity may favour alleles at adaptive loci like the Major Histocompatibility Complex (MHC) that are maladaptive in natural environments. We investigated neutral and MHC-linked genetic variation in three autochthonous and three hatchery populations of Austrian brown trout (Salmo trutta). We confirm a positive selection pressure acting on the MHC II β locus, whereby the signal for positive selection was stronger in hatchery versus wild populations. Additionally, diversity at the MHC II β locus was higher, and more uniform among hatchery samples compared to wild populations, despite equal levels of diversity at neutral loci. We postulate that this stems from a combination of stronger genetic drift and a weakening of positive selection at this locus in wild populations that already have well adapted alleles for their specific environments.     

Why do salmonid antipredator responses weaken in hatchery rearing?

The Arctic charr of Lake Saimaa are the most endangered fish population in Finland, and reintroduction programs have been unsuccessful. Low success of reintroduction programs has drawn attention to behavioural properties of hatcheryreared fish. Mortality due to predation often is a principal cause of failure. Antipredator behaviour may degenerate rapidly under hatchery conditions due to (i) reduced genetic variation in antipredator behaviour and/or (ii) selection that would favour bold and fast growing individuals and disfavour predator awareness supposedly associated with slow growth. To test the relative importance of these two factors we first analysed the amount of variation in innate antipredator responses between and within families of hatchery‐bred Arctic charr of the Lake Saimaa stock. We then tested whether fast growing individuals would show reduced responses to chemical cues from their natural predators compared to their slow growing counterparts. Based on the results we propose procedures for maintaining and improving antipredator skills of hatchery‐reared salmonids.     

Nestling growth in the Great Tit I. Heritability estimates under different environmental conditions

Evolutionary change requires natural selection in the presence of heritable variation for the trait(s) under selection. Since heritabilities and selection pressures are known to vary with environmental conditions, it is crucial to know how much genetic variation is expressed under which conditions. This study addresses the question of how the expression of genetic variation for fledgling body size of Great Tits varies with the environment. Different environmental conditions were created experimentally by manipulating brood sizes. The treatment affected body size, measured as either fledging weight or tarsus length, and interacted with natural temporal variation in food availability. Both measurements show stabilizing selection. A cross-fostering design was carried out to separate genetic and environmental causes of variation. Heritabilities as measured from offspring-midparent regressions and from full-sib analyses were substantial for both traits, except that no heritability was found for weight under poor conditions. Instead, fledging weights were significantly correlated with the weights of their unrelated guardians' ( = fosterparents') weight under poor conditions. We propose that under poor conditions, when selection on fledging weights is expected to be directional and strong, only little genetic variance is expressed. Any evolutionary response to this selection on fledging weight might therefore be slow, if the increase in selection pressure is not greater than the decrease in heritability.     

Anti‐predatory behaviour of wild‐caught vs captive‐bred freshwater angelfish,Pterophyllum scalare

Environments and experiences encountered in early life stages of animals shape their adult behaviour. When environments are maintained for several generations, differential selection forces act upon individuals to select those most fit to the particular conditions. As such, differences in the behaviour of captive bred and wild caught individuals have been observed recurrently. In fish, hatchery raised individuals tend to seek refuge less, making them more vulnerable to predators. We tested the hypothesis that captive breeding induces non‐adaptive changes in behaviour of freshwater angelfish, Pterophyllum scalare. Wild‐caught and captive‐bred fish were exposed to a natural predator and measured for their anti‐predator behaviours; no differences were found in behaviour under control conditions. When exposed to a natural predator, wild‐caught fish exhibited significantly shorter freezing durations than captive‐bred fish, and took significantly shorter time to resume normal behaviour. No differences in the time taken to initiate investigations of the predator were detected. The results demonstrate that captive‐bred fish respond differently than their wild counterparts when exposed to a natural predator, and that this domestication has implications for captive rearing programmes.     

Heritability and social brood effects on personality in juvenile and adult life‐history stages in a wild passerine

How has evolution led to the variation in behavioural phenotypes (personalities) in a population? Knowledge of whether personality is heritable, and to what degree it is influenced by the social environment, is crucial to understanding its evolutionary significance, yet few estimates are available from natural populations. We tracked three behavioural traits during different life‐history stages in a pedigreed population of wild house sparrows. Using a quantitative genetic approach, we demonstrated heritability in adult exploration, and in nestling activity after accounting for fixed effects, but not in adult boldness. We did not detect maternal effects on any traits, but we did detect a social brood effect on nestling activity. Boldness, exploration and nestling activity in this population did not form a behavioural syndrome, suggesting that selection could act independently on these behavioural traits in this species, although we found no consistent support for phenotypic selection on these traits. Our work shows that repeatable behaviours can vary in their heritability and that social context influences personality traits. Future efforts could separate whether personality traits differ in heritability because they have served specific functional roles in the evolution of the phenotype or because our concept of personality and the stability of behaviour needs to be revised.     

The behavioural response of Great Tits to novel environment and handling is affected by the DRD4 gene

Studies have provided inconsistent evidence regarding the effects on behaviour of nucleotide polymorphism at the DRD4 gene. For instance, the DRD4 gene affects exploratory behaviour in some bird species and populations but not in others. Our earlier experiment with a wild Great Tit Parus major population revealed an important impact of the DRD4 gene on behavioural variation during the breeding season. The aim of this study was to clarify these results by measuring individual behavioural differences (exploration and anxiety) in Great Tits under controlled conditions before the beginning of egg‐laying in order to exclude the potential impacts of breeding (egg‐laying, motivation to feed nestlings, the potential effect of a partner) and the natural environment (e.g. the presence of predators). Birds were caught from their natural habitat and their behaviour was tested in a trial room the following morning. Individuals with the CT heterozygous genotype (SNP830) performed more actively in different contexts (visiting a novel object in the trial room and vocal behaviour during handling) compared with homozygotes, and the relationships were consistent in males and females. In light of the results from our previous study (heterozygous males, but not females, had a shorter latency to feed nestlings than CC homozygotes), we conclude that the same DRD4 gene variants affect behavioural responses in a controlled environment and wild contexts in the same directions, but that these relationships are not sex‐specific under standardized conditions.     

Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki)

Correlated traits are important from an evolutionary perspective as natural selection acting on one trait may indirectly affect other traits. Further, the response to selection can be constrained or hastened as a result of correlations. Because mating behaviour and body colour can dramatically affect fitness, a correlation between them can have important fitness ramifications. In this work, melanic (black) male mosquitofishes (Gambusia holbrooki) with temperature-sensitive body-colour expression are bred in captivity. Half of the sons of each melanic sire are reared at 19 degrees C (and express a black body colour) and half are reared at 31 degrees C (and express a silver body colour). The two colour morphs are placed in the same social setting and monitored for behavioural differences. Mating behaviour and colour are correlated traits. Mating behaviour differs markedly between the two phenotypes, despite high genetic relatedness. Melanic (black) phenotypes are more aggressive towards females, chasing them and attempting more matings than their silver siblings. Females avoid melanic-male mating attempts more than silver-male mating attempts. When males with temperature-sensitive colour expression are melanic and aggressive, they probably experience a very different selective regime in nature from when they are silver and less aggressive. Under some conditions (e.g. predation), melanic coloration and/or aggression is advantageous compared with silver coloration and/or less aggressive behaviour. However, under different conditions (e.g. high-frequency melanism), melanism and/or aggression appears to be disadvantageous and melanic males have reduced survival and reproduction. Selective advantages to each morph under different conditions may enable the long-term persistence of this temperature-sensitive genotype.     

Experimental evolution of infectious behaviour in a facultative ectoparasite

Parasitic lifestyles have evolved many times in animals, but how such life‐history strategies evolved from free‐living ancestors remains a great puzzle. Transitional symbiotic strategies, such as facultative parasitism, are hypothesized evolutionary stepping stones towards obligate parasitism. However, to consider this hypothesis, heritable genetic variation in infectious behaviour of transitional symbiotic strategies must exist. In this study, we experimentally evolved infectivity and estimated the additive genetic variation in a facultative parasite. We performed artificial selection experiments in which we selected for either increased or decreased propensity to infect in a facultatively parasitic mite (Macrocheles muscaedomesticae). Here, infectiousness was expressed in terms of mite attachment to a host (Drosophila hydei) and modelled as a threshold trait. Mites responded positively to selection for increased infectivity; realized heritability of infectious behaviour was significantly different from zero and estimated to be 16.6% (±4.4% SE). Further, infection prevalence was monitored for 20 generations post‐selection. Selected lines continued to display relatively high levels of infection, demonstrating a degree of genetic stability in infectiousness. Our study is the first to provide an estimate of heritability and additive genetic variation for infectious behaviour in a facultative parasite, which suggests natural selection can act upon facultative strategies with important implications for the evolution of parasitism.     

The heritability of multiple male mating in a promiscuous mammal

The tendency of females to mate with multiple males is often explained by direct and indirect benefits that could outweigh the many potential costs of multiple mating. However, behaviour can only evolve in response to costs and benefits if there is sufficient genetic variation on which selection can act. We followed 108 mating chases of 85 North American red squirrels (Tamiasciurus hudsonicus) during 4 years, to measure each female's degree of multiple male mating (MMM), and used an animal model analysis of our multi-generational pedigree to provide what we believe is the first estimate of the heritability of MMM in the wild. Female red squirrels were highly polyandrous, mating with an average of 7.0 ± 0.2 males on their day of oestrus. Although we found evidence for moderate levels of additive genetic variation (CV(A) = 5.1), environmental variation was very high (CV(E) = 32.3), which resulted in a very low heritability estimate (h(2) < 0.01). So, while there is genetic variation in this trait, the large environmental variation suggests that any costs or benefits associated with differences among females in MMM are primarily owing to environmental and not genetic differences, which could constrain the evolutionary response to natural selection on this trait.     

Effect of captivity on genetic variance for five traits in the large milkweed bug (Oncopeltus fasciatus)

Understanding the changes in genetic variance which may occur as populations move from nature into captivity has been considered important when populations in captivity are used as models of wild ones. However, the inherent significance of these changes has not previously been appreciated in a conservation context: are the methods aimed at founding captive populations with gene diversity representative of natural populations likely also to capture representative quantitative genetic variation? Here, I investigate changes in heritability and a less traditional measure, evolvability, between nature and captivity for the large milkweed bug, Oncopeltus fasciatus, to address this question. Founders were collected from a 100-km transect across the north-eastern US, and five traits (wing colour, pronotum colour, wing length, early fecundity and later fecundity) were recorded for founders and for their offspring during two generations in captivity. Analyses reveal significant heritable variation for some life history and morphological traits in both environments, with comparable absolute levels of evolvability across all traits (0-30%). Randomization tests show that while changes in heritability and total phenotypic variance were highly variable, additive genetic variance and evolvability remained stable across the environmental transition in the three morphological traits (changing 1-2% or less), while they declined significantly in the two life-history traits (5-8%). Although it is unclear whether the declines were due to selection or gene-by-environment interactions (or both), such declines do not appear inevitable: captive populations with small numbers of founders may contain substantial amounts of the evolvability found in nature, at least for some traits.     

Inter-Population Variation in Hoarding Behaviour in Degus, Octodon degus

Although foraging comprises a set of behaviours that typically vary with resource availability and/or climatic conditions, few studies have analysed how foraging, particularly food hoarding, varies across populations inhabiting different habitats. We carried out an inter-population study on foraging behaviour with the caviomorph rodent Octodon degus collected from two geographically separated populations in central Chile, with contrasting climates. One population was located in a mountainous zone (at 2600 m elevation) characterized by a high-altitude climate. The other population was from a low-altitude Mediterranean climate zone (450 m elevation). Under laboratory conditions, we measured population-specific differences in food consumption and hoarding by recording food utilization. We also assessed whether acclimation played a role in behavioural differences, by using two different sets of animals that had been in captivity for (1) 2 wk or (2) 6 mo, under common conditions. The results showed variation in food hoarding between populations. Individuals from the low-altitude population exclusively displayed scatter hoarding behaviour. In contrast, high-altitude animals carried out larder hoarding combined with scatter hoarding (37.4% and 62.6% respectively). There was no intra-population variation between degus with different acclimation periods under captivity, thus inter-population differences in larder hoarding were maintained despite 6 mo of acclimation to a common environment. The geographic variation observed suggests that larder hoarding is favoured under harsher environmental conditions. We discuss some probable causes for this variation. The lack of effect of acclimation suggests that inter-population differences in larder hoarding might be the result of local adaptation or, less likely, it corresponds to an ontogenetically acquired irreversible behaviour.     

Fitness consequences of avian personalities in a fluctuating environment

Individual animals differ in the way they cope with challenges in their environment, comparable with variation in human personalities. The proximate basis of variation in personality traits has received considerable attention, and one general finding is that personality traits have a substantial genetic basis. This poses the question of how variation in personality is maintained in natural populations. We show that selection on a personality trait with high heritability fluctuates across years within a natural bird population. Annual adult survival was related to this personality trait (behaviour in novel environments) but the effects were always opposite for males and females, and reversed between years. The number of offspring surviving to breeding was also related to their parents' personalities, and again selection changed between years. The observed annual changes in selection pressures coincided with changes in environmental conditions (masting of beeches) that affect the competitive regimes of the birds. We expect that the observed fluctuations in environmental factors lead to fluctuations in competition for space and food, and these, in association with variations in population density, lead to a variation in selection pressure, which maintains genetic variation in personalities.     

Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges

Cognition is defined as the processes by which animals collect, retain and use information from their environment to guide their behaviour. Thus cognition is essential in a wide range of behaviours, including foraging, avoiding predators and mating. Despite this pivotal role, the evolutionary processes shaping variation in cognitive performance among individuals in wild populations remain very poorly understood. Selection experiments in captivity suggest that cognitive traits can have substantial heritability and can undergo rapid evolution. However only a handful of studies have attempted to explore how cognition influences life‐history variation and fitness in the wild, and direct evidence for the action of natural or sexual selection on cognition is still lacking, reasons for which are diverse. Here we review the current literature with a view to: (i) highlighting the key practical and conceptual challenges faced by the field; (ii) describing how to define and measure cognitive traits in natural populations, and suggesting which species, populations and cognitive traits might be examined to greatest effect; emphasis is placed on selecting traits that are linked to functional behaviour; (iii) discussing how to deal with confounding factors such as personality and motivation in field as well as captive studies; (iv) describing how to measure and interpret relationships between cognitive performance, functional behaviour and fitness, offering some suggestions as to when and what kind of selection might be predicted; and (v) showing how an evolutionary ecological framework, more generally, along with innovative technologies has the potential to revolutionise the study of cognition in the wild. We conclude that the evolutionary ecology of cognition in wild populations is a rapidly expanding interdisciplinary field providing many opportunities for advancing the understanding of how cognitive abilities have evolved.