Personality and urbanization: behavioural traits and <Emphasis Type="Italic">DRD4</Emphasis> SNP830 polymorphisms in great tits in Barcelona city

Most examples of adaptation to the urban environment relate to plasticity processes rather than to natural selection. Personality, however, defined as consistent individual differences in behaviour related to exploration, caution, and neophobia, is a good behavioural candidate character to study natural selection in relation to the urban habitat due to its heritable variation. The aim of this paper was to analyse variation in personality by comparing urban and forest great tits Parus major using standard tests of exploratory behaviour and boldness. We studied personality in 130 wild great tits captured in Barcelona city and nearby forests and found that urban birds were more explorative and bolder towards a novel object than forest birds. Genotype frequencies of the DRD4 SNP830 polymorphism, a gene region often associated with personality variation, varied significantly between forest and urban birds. Behavioural scores, however, were not correlated with this polymorphism in our population. Exploration scores correlated to boldness for forest birds but not for urban birds. Our findings suggest that the novel selection pressures of the urban environment favour the decoupling of behavioural traits that commonly form behavioural syndromes in the wild.     

Personality and basal metabolic rate in a wild bird population

Personality and metabolic rate are predicted to show covariance on methodological and functional grounds, but empirical studies at the individual level are rare, especially in natural populations. Here we assess the relationship between exploration behaviour, an important axis of personality, and basal metabolic rate (BMR) for 680 free‐living great tits Parus major, studied over three years. We find that exploration behaviour is weakly negatively related to BMR among female, but not male, birds. Moreover, we find exploration behaviour to be independent of methodological aspects of BMR measurements (e.g. activity levels, time to acclimatize) which have been suggested to be indicative of personality‐related activity or stress levels during measurement. This suggests that the weak link between exploration behaviour and BMR found here is functional rather than methodological. We therefore test the hypothesis that selection favours covariance between exploration behaviour and metabolic rate, but find no evidence for correlational survival or fecundity selection. Our data therefore provide at best only very weak evidence for a functional link between personality and metabolic rate, and we suggest that studies of personality and metabolic strategies, or personality and daily energy expenditure, are required to further resolve the link between personality and metabolic rate.     

Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in Great tit nestlings, Parus major

In nestlings, glucocorticoid (GC) secretion has short-term and long-term f itness consequences. For example, short-time elevations trigger begging activity, whereas chronically elevated GC levels impair body condition, growth and cognitive abilities. Despite a growing body of literature on personality traits, the effects of selection for fast and slow exploration on GC secretion have received little attention. We compared baseline and stress-induced hypothalamic–pituitary–adrenal (HPA) axis activity of hand-reared great tit nestlings of lines selected for fast and slow exploration. Nestling droppings were collected under three conditions: control, test (following handling stress, day 14 after hatching) and the following day. The concentrations of excreted immunoreactive corticosterone metabolites (CM) were determined via an enzyme immunoassay. We also observed nestlings' begging behaviour. CM differed significantly between the lines. Nestlings of the fast line excreted lower CM than slow-line birds. In response to handling stress, nestlings excreted significantly higher concentrations of CM than during the control and on the day after handling. Sex and begging activity were not related to CM levels. Under the control condition, but not after handling, males begged significantly more often than females. In both lines, adults excreted significantly less CM compared to nestlings. Both nestlings and adults of the slow line produced higher baseline CM values than fast-line birds. Fast-line nestlings excreted lower baseline CM than nestlings of a wild population not selected for fast or slow exploration. Slow-line nestlings did not. Our results show that selection on the basis of exploratory behaviour affected HPA axis reactivity.     

Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in Great tit nestlings,Parus major

In nestlings, glucocorticoid (GC) secretion has short-term and long-term f itness consequences. For example, short-time elevations trigger begging activity, whereas chronically elevated GC levels impair body condition, growth and cognitive abilities. Despite a growing body of literature on personality traits, the effects of selection for fast and slow exploration on GC secretion have received little attention. We compared baseline and stress-induced hypothalamic–pituitary–adrenal (HPA) axis activity of hand-reared great tit nestlings of lines selected for fast and slow exploration. Nestling droppings were collected under three conditions: control, test (following handling stress, day 14 after hatching) and the following day. The concentrations of excreted immunoreactive corticosterone metabolites (CM) were determined via an enzyme immunoassay. We also observed nestlings' begging behaviour. CM differed significantly between the lines. Nestlings of the fast line excreted lower CM than slow-line birds. In response to handling stress, nestlings excreted significantly higher concentrations of CM than during the control and on the day after handling. Sex and begging activity were not related to CM levels. Under the control condition, but not after handling, males begged significantly more often than females. In both lines, adults excreted significantly less CM compared to nestlings. Both nestlings and adults of the slow line produced higher baseline CM values than fast-line birds. Fast-line nestlings excreted lower baseline CM than nestlings of a wild population not selected for fast or slow exploration. Slow-line nestlings did not. Our results show that selection on the basis of exploratory behaviour affected HPA axis reactivity.     

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.     

Personality drives physiological adjustments and is not related to survival

The evolutionary function and maintenance of variation in animal personality is still under debate. Variation in the size of metabolic organs has recently been suggested to cause and maintain variation in personality. Here, we examine two main underlying notions: (i) that organ sizes vary consistently between individuals and cause consistent behavioural patterns, and (ii) that a more exploratory personality is associated with reduced survival. Exploratory behaviour of captive red knots (Calidris canutus, a migrant shorebird) was negatively rather than positively correlated with digestive organ (gizzard) mass, as well as with body mass. In an experiment, we reciprocally reduced and increased individual gizzard masses and found that exploration scores were unaffected. Whether or not these birds were resighted locally over the 19 months after release was negatively correlated with their exploration scores. Moreover, a long-term mark–recapture effort on free-living red knots with known gizzard masses at capture confirmed that local resighting probability (an inverse measure of exploratory behaviour) was correlated with gizzard mass without detrimental effects on survival. We conclude that personality drives physiological adjustments, rather than the other way around, and suggest that physiological adjustments mitigate the survival costs of exploratory behaviour. Our results show that we need to reconsider hypotheses explaining personality variation based on organ sizes and differential survival.     

Realized heritability of personalities in the great tit (Parus major)

Behaviour under conditions of mild stress shows consistent patterns in all vertebrates: exploratory behaviour, boldness, aggressiveness covary in the same way. The existence of highly consistent individual variation in these behavioural strategies, also referred to as personalities or coping styles, allows us to measure the behaviour under standardized conditions on birds bred in captivity, link the standardized measurements to the behaviour under natural conditions and measure natural selection in the field. We have bred the great tit (Parus major), a classical model species for the study of behaviour under natural conditions, in captivity. Here, we report a realized heritability of 54 +/- 5% for early exploratory behaviour, based on four generations of bi-directional artificial selection. In addition to this, we measured hand-reared juveniles and their wild-caught parents in the laboratory. The heritability found in the mid-offspring-mid-parent regression was significantly different from zero. We have thus established the presence of considerable amounts of genetic variation for personality types in a wild bird.     

Additive and nonadditive genetic variation in avian personality traits

Individuals of all vertebrate species differ consistently in their reactions to mildly stressful challenges. These typical reactions, described as personalities or coping strategies, have a clear genetic basis, but the structure of their inheritance in natural populations is almost unknown. We carried out a quantitative genetic analysis of two personality traits (exploration and boldness) and the combination of these two traits (early exploratory behaviour). This study was carried out on the lines resulting from a two-directional artificial selection experiment on early exploratory behaviour (EEB) of great tits (Parus major) originating from a wild population. In analyses using the original lines, reciprocal F(1) and reciprocal first backcross generations, additive, dominance, maternal effects ands sex-dependent expression of exploration, boldness and EEB were estimated. Both additive and dominant genetic effects were important determinants of phenotypic variation in exploratory behaviour and boldness. However, no sex-dependent expression was observed in either of these personality traits. These results are discussed with respect to the maintenance of genetic variation in personality traits, and the expected genetic structure of other behavioural and life history traits in general.     

Personality and Information Gathering in Free-Ranging Great Tits

One aspect of animal personality that has been well described in captivity, but received only little attention in studies in the wild, is that personality types may vary in their behavioural flexibility towards environmental changes. A fundamental factor underlying such differences is believed to be the degree to which individual behavior is guided by environmental stimuli. We tested this hypothesis in the wild using free-ranging great tits. Personality variation was quantified using exploratory behaviour in a novel environment, which has previously been shown to be repeatable and correlated with other behaviours in this and other populations of the same species. By temporarily removing food at feeding stations we examined whether birds with different personality differed in returning to visit empty feeders as this may provide information on how birds continue to sample their environment after a sudden change in conditions. In two summer experiments, we found that fast-exploring juveniles visited empty feeders less often compared to slow-exploring juveniles. In winter, sampling behaviour was sex dependent but not related to personality. In both seasons, we found that birds who sampled empty feeders more often were more likely to rediscover food after we again re-baited the feeding stations, but there was no effect of personality. Our results show that personality types may indeed differ in ways of collecting environmental information, which is consistent with the view of personalities as different styles of coping with environmental changes. The adaptive value of these alternative behavioural tactics, however, needs to be further explored.     

Personality and Nest Defence in the Great Tit (Parus major)

A growing number of studies have shown that individuals differ consistently in a suite of correlated behavioural traits across various contexts and situations. Yet, most work on animal personalities has been performed under laboratory conditions and still little is known about the ecological significance of differences in personality in the wild, and the behavioural mechanisms underlying possible fitness consequences. In this study, we investigated individual differences in personality in relation to nest defence behaviour in wild great tits. Nest defence is an important aspect of parental care and involves a trade‐off between two fitness components (i.e. survival and reproduction). As a measure of personality we used exploratory behaviour in a novel environment as this has been shown to be correlated with several other behavioural traits including risk‐taking and aggression, two important behavioural components of nest defence. We found that the intensity of alarm calling towards a human intruder was positively associated with exploratory behaviour, while there was a negative association between exploration score and number of movements during nest defence. Thus, fast explorers are shown to respond more boldly towards predators in the field. More generally we show that individuals with different personalities vary in their anti‐predator and reproductive investment strategies.     

Density fluctuations represent a key process maintaining personality variation in a wild passerine bird

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.     

Natural selection,plasticity and the emergence of a behavioural syndrome in the wild

Individuals often show consistent behavioural differences where behaviours can form integrated units across functionally different contexts. However, the factors causing and maintaining behavioural syndromes in natural populations remain poorly understood. In this study, we provide evidence for the emergence of a behavioural syndrome during the first months of life in wild brown trout (Salmo trutta). Behavioural traits of trout were scored before and after a 2‐month interval covering a major survival bottleneck, whereupon the consistency and covariance of behaviours were analysed. We found that selection favoured individuals with high activity levels in an open‐field context, a personality trait consistent throughout the duration of the experiment. In addition, a behavioural syndrome emerged over the 2 months in the wild, linking activity to aggressiveness and exploration tendency. These novel results suggest that behavioural syndromes can emerge rapidly in nature from interaction between natural selection and behavioural plasticity affecting single behaviours.     

Heritability and genetic correlations of personality traits in a wild population of yellow‐bellied marmots (Marmota flaviventris)

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 nonzero additive genetic variance in these traits. We also found nonzero 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.     

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.     

Personality and innate immune defenses in a wild bird: Evidence for the pace-of-life hypothesis

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.     

Disruptive viability selection on adult exploratory behaviour in eastern chipmunks

Heterogeneous forces of selection associated with fluctuating environments are recognized as important factors involved in the maintenance of inter‐individual phenotypic variance within populations. Consistent behavioural differences over time and across situations (e.g. personality) are increasingly cited as examples of individual variation observed within populations. However, the suggestion that heterogeneous selective pressures target different animal personalities remains largely untested in the wild. In this 5‐year study, we investigated the dynamics of viability selection on a personality trait, exploration, in a population of eastern chipmunks (Tamias striatus) experiencing substantial seasonal variations in weather conditions and food availability associated with masting trees. Contrary to our expectations, we found no evidence of fluctuating selection on exploration. Instead, we found strong disruptive viability selection on adult exploration behaviour, independent of seasonal variations. Individuals with either low or high exploration scores were almost twice as likely to survive over a 6‐month period compared with individuals with intermediate scores. We found no evidence of viability selection on juvenile exploration. Our results highlight that disruptive selection might play an important role in the maintenance of phenotypic variance of wild populations through its effect on different personality types across temporally varying environmental conditions.     

Exploratory behavior undergoes genotype–age interactions in a wild bird

Animal personality traits are often heritable and plastic at the same time. Indeed, behaviors that reflect an individual's personality can respond to environmental factors or change with age. To date, little is known regarding personality changes during a wild animals' lifetime and even less about stability in heritability of behavior across ages. In this study, we investigated age‐related changes in the mean and in the additive genetic variance of exploratory behavior, a commonly used measure of animal personality, in a wild population of great tits. Heritability of exploration is reduced in adults compared to juveniles, with a low genetic correlation across these age classes. A random regression animal model confirmed the occurrence of genotype–age interactions (G×A) in exploration, causing a decrease in additive genetic variance before individuals become 1 year old, and a decline in cross‐age genetic correlations between young and increasingly old individuals. Of the few studies investigating G×A in behaviors, this study provides rare evidence for this phenomenon in an extensively studied behavior. We indeed demonstrate that heritability and cross‐age genetic correlations in this behavior are not stable over an individual's lifetime, which can affect its potential response to selection. Because G×A is likely to be common in behaviors and have consequences for our understanding of the evolution of animal personality, more attention should be turned to this phenomenon in the future work.     

The relation between dominance and exploratory behavior is context-dependent in wild great tits

Individual differences in personality affect behavior in novelor challenging situations. Personality traits may be subjectto selection because they affect the ability to dominate others.We investigated whether dominance rank at feeding tables inwinter correlated with a heritable personality trait (as measuredby exploratory behavior in a novel environment) in a naturalpopulation of great tits, Parus major. We provided clumped resourcesat feeding tables and calculated linear dominance hierarchieson the basis of observations between dyads of color-ringed individuals,and we used an experimental procedure to measure individualexploratory behavior of these birds. We show that fast-exploringterritorial males had higher dominance ranks than did slow-exploringterritorial males in two out of three samples, and that dominancerelated negatively to the distance between the site of observationand the territory. In contrast, fast-exploring nonterritorialjuveniles had lower dominance ranks than did slow-exploringnonterritorial juveniles, implying that the relation betweendominance and personality is context-dependent in the wild.We discuss how these patterns in dominance can explain earlierreported effects of avian personality on natal dispersal andfitness.     

Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty‐seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab‐raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free‐living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free‐living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5–5.8% of the total variance—a large effect for a single gene influencing a complex behavioural trait—but not in three others. The confirmation of an association between SNP830 genotype and personality‐related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.     

The influence of spatiotemporal conditions and personality on survival in reintroductions–evolutionary implications

Personality exists in non-human animals and can impact fitness. There is, however, a shortage of empirical studies in certain areas within the field, and fundamental evolutionary theory on personality remains largely untested. For example, little is known on how variation in personality is maintained over evolutionary time. Theory suggests that fluctuating selection pressures due to spatiotemporal variation in conditions, e.g. food availability, is a possible mechanism and a few studies have shown that the success of different personality types varies with spatiotemporal conditions. However, it remains unknown whether different mechanisms can maintain personality within a species. Here we use a reintroduction programme for the critically endangered European mink (Mustela lutreola) to test whether multiple personality trait domains (boldness, exploration and sociability) affected survival in two different years and islands. This was done through pre-release personality tests and post-release radio-tracking monitoring. Survival was positively correlated with boldness, whereas the relationship with exploration was either negative or positive depending on year/island. The results show a complex relationship between personality and survival and suggest that exploration can be maintained over evolutionary time via spatiotemporal variation in conditions. However, in contrast to exploration, boldness did not vary spatiotemporally and sociability had no impact on survival. This indicates that different personality trait domains might be maintained by different mechanisms. To date, personality has been studied primarily within behavioural sciences, but through empirical findings we highlight the importance of personality also in ecology and conservation biology.