Evolutionary quantitative genetics of behavioral responses to handling in a wild passerine

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 (h² = 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.     

A multi-trait,field-based examination of personality in a semi-aquatic turtle

Studies documenting and quantifying personality traits are common in animal behavior. Such studies often consider the nature of individual variation and personality as correlated with a variety of natural history, physiological, or ecological traits, and therefore consider the importance of personality for strategies in wild systems. Though such studies have contributed markedly to our understanding of the important aspects of personality that may covary with a variety of factors that might affect fitness, much of the research on animal personalities is taxonomically limited. To supplement and compliment the laboratory study of reptile personality, we examined the patterns of multiple personality traits in wild Eastern painted turtles (Chrysemys picta) in the field. We examined patterns of aggression, sociability, and boldness across these traits in different contexts in 103 adult, wild-caught turtles. We found strong correlations both within and among the focal behavioral axes, representing robust evidence for personality in this species. Specifically, we found strong relationships among many measures of aggression, as well as relationships between aggression and our measures of boldness. Finally, we note a tendency for sociability in our turtles, with animals scoring high on sociability showing lower tendency toward aggression. Overall, our study provides robust evidence for correlated suites of behavioral traits, or personality, in a semi-aquatic turtle surveyed in the wild. Future work should continue to expand the range of traits examined to more fully consider the ecological consequences of variation in personality in this and similar species.     

Female aggression predicts mode of paternity acquisition in a social lizard

Individual differences in behaviour are ubiquitous in nature. Despite the likely role of selection in maintaining these differences, there are few demonstrations of their fitness consequences in wild populations and, consequently, the mechanisms that link behavioural variation to variation in fitness are poorly understood. Specifically, the consequences of consistent individual differences in behaviour for the evolution of social and mating strategies have rarely been considered. We examined the functional links between variation in female aggression and her social and mating strategies in a wild population of the social lizard Egernia whitii. We show that female Egernia exhibit temporally consistent aggressive phenotypes, which are unrelated to body size, territory size or social density. A female''s aggressive phenotype, however, has strong links to her mode of paternity acquisition (within- versus extra-pair paternity), with more aggressive females having more offspring sired by extra-pair males than less aggressive females. We discuss the potential mechanisms by which female aggression could underpin mating strategies, such as the pursuit/acceptance of extra-pair copulations. We propose that a deeper understanding of the evolution and maintenance of social and mating systems may result from an explicit focus on individual-level female behavioural phenotypes and their relationship with key reproductive strategies.     

Social personality trait and fitness

Several recent studies have explored various aspects of animal personality and their ecological consequences. However, the processes responsible for the maintenance of personality variability within a population are still largely unknown. We have recently demonstrated that social personality traits exist in the common lizard (Lacerta vivipara) and that the variation in sociability provides an explanation for variable dispersal responses within a given species. However, we need to know the fitness consequences of variation in sociability across environmental contexts in order to better understand the maintenance of such variation. In order to achieve this, we investigated the relationship between sociability and survival, body growth and fecundity, in one-year-old individuals in semi-natural populations with varying density. 'Asocial' and 'social' lizards displayed different fitness outcomes in populations of different densities. Asocial lizards survived better in low-density populations, while social females reproduced better. Spatiotemporal variation in environmental conditions might thus be the process underlying the maintenance of these personality traits within a population. Finally, we also discuss the position of sociability in a more general individual behavioural pattern including boldness, exploration and aggressiveness.     

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.     

Habitat selection and potential fitness consequences of two early‐successional species with differing life‐history strategies

Habitat selection and its relationship to fitness is a fundamental concept in ecology, but the mechanisms driving this connection are complex and difficult to detect. Despite the difficulties in understanding such intricate relationships, it is imperative that we study habitat selection and its relationship with fitness. We compared habitat selection of least terns (Sternula antillarum) and piping plovers (Charadrius melodus) on the Missouri River (2012–2014) to examine the consequences of those choices on nest and chick survival. We hypothesized that plovers and terns would select habitat that minimized the chance of flooding and predation of eggs, chicks, and adults, but that plovers would also select habitat that would provide foraging habitat for their chicks. We developed an integrated habitat selection model that assessed selection across multiple scales (sandbar and nest scales) and directly modeled the effect of selection on nest and chick survival. In general, the species selected habitat in keeping with our hypotheses, such that predation and flooding, in particular, may have been reduced. Sandbar selection had either a negative or no appreciable effect on nest survival for both species across years. Nest‐site selection in 2012 had a generally positive effect on nest survival and chick survival for both terns and plovers, and this trended toward a negative effect by 2014. This result suggested that early selection decisions appeared to be adaptive, but we speculate that relatively high site fidelity and habitat degradation led to reduced benefit over time. Our results highlight the complex nature of habitat selection and its relationship to fitness.     

Repeatable intra-individual variation in plasma testosterone concentration and its sex-specific link to aggression in a social lizard

Individual hormone profiles can be important generators of phenotypic variation. Despite this, work on the consequences of hormone profiles has traditionally ignored the large inter-individual variation within natural populations. However, recent research has advocated the need to explicitly consider this variation and address its consequences for selection. One of the key steps in this process is examining repeatability in hormone profiles and their links to behavioral traits under selection. In this study we show that individuals within a free-ranging population of the Australian lizard Egernia whitii exhibit temporal repeatability in their circulating baseline testosterone concentrations as well as their aggressive response towards conspecific intruders. Furthermore, we show significant, sex-specific links between testosterone and aggression. Specifically, testosterone and aggression is negatively linked in males, while there is no relationship in females. As conspecific aggression has significant consequences for fitness-related traits (parental care, mating strategies) in this species, inter-individual variation in testosterone concentrations, through their effects on aggression, could have important implications for individual fitness. We discuss the potential causes and consequences of hormonal repeatability as well as provide explanations for its sex-specific links with aggression. Specifically, we suggest that these patterns are the result of alternative hormonal pathways governing aggression within Egernia and may indicate a decoupling of aggression and testosterone across the sexes.     

What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the ‘maintenance costs’ of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.     

Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output

There is growing evidence that behavioral tendencies, or “personalities,” in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality.     

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.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

Individual variation in social aggression and the probability of inheritance: theory and a field test

Recent theory suggests that much of the wide variation in individual behavior that exists within cooperative animal societies can be explained by variation in the future direct component of fitness, or the probability of inheritance. Here we develop two models to explore the effect of variation in future fitness on social aggression. The models predict that rates of aggression will be highest toward the front of the queue to inherit and will be higher in larger, more productive groups. A third prediction is that, in seasonal animals, aggression will increase as the time available to inherit the breeding position runs out. We tested these predictions using a model social species, the paper wasp Polistes dominulus. We found that rates of both aggressive "displays" (aimed at individuals of lower rank) and aggressive "tests" (aimed at individuals of higher rank) decreased down the hierarchy, as predicted by our models. The only other significant factor affecting aggression rates was date, with more aggression observed later in the season, also as predicted. Variation in future fitness due to inheritance rank is the hidden factor accounting for much of the variation in aggressiveness among apparently equivalent individuals in this species.     

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy “within” the group is also the most detrimental strategy “for” the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex‐ratio among groups, thereby increasing the importance of between‐group selection compared to within‐group selection. Females dispersed away from local aggression, creating more favorable mating environments for less‐aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.     

Can natural selection maintain long-distance dispersal? Insight from a stream salamander system

Dispersal distributions are often characterized by many individuals that stay close to their origin and large variation in the distances moved by those that leave. This variation in dispersal distance can strongly influence demographic, ecological, and evolutionary processes. However, a lack of data on the fitness and phenotype of individual dispersers has impeded research on the role of natural selection in maintaining variation in dispersal distance. Six years of spatially explicit capture-mark-recapture data showed that survival increased with dispersal distance in the stream salamander Gyrinophilus porphyriticus. To understand the evolutionary implications of this fitness response, we tested whether variation in dispersal distance has a phenotypic basis. We used photographs of marked individuals to measure head, trunk, and leg morphology. We then tested whether dispersal distances over the six-year study period were predicted by these traits. Dispersal distance was significantly related to leg morphology: individuals with relatively long forelimbs and short hindlimbs dispersed the farthest. These results support the hypothesis that positive fitness consequences maintain phenotypes enabling long-distance dispersal. More broadly, they suggest that natural selection can promote variation in dispersal distance and associated phenotypes, offering an alternative to the view that dispersal distance is driven by stochastic or landscape-specific mechanisms.     

动物个性研究进展

"个性"是指不同时空条件下动物种群个体间行为的稳定差异。大量的理论和实验性研究表明,个性差异在动物界普遍存在,其是种群多度和分布、物种共存及群落构建的重要驱动因子。介绍了动物个性的概念、分类及衡量指标,将前人测量个性类型的方法加以总结;随后介绍了动物个性的生态学意义,尤其是个性对动物生活史策略、种群分布与多度、群落结构和动态、生态系统功能和过程以及疾病与信息传播等的影响。在此基础上,进一步分析了在人类活动增加等全球变化背景下,动物个性如何调控动物个体行为、种群和群落动态对这些环境变化的响应。阐述了动物个性的形成与维持机制,并对未来的研究方向进行了展望。     

The interaction between personality, offspring fitness and food abundance in North American red squirrels

Animal personality is now frequently reported in wild and captive populations. It has been shown to be moderately heritable and to have potentially important fitness consequences. Variation in personality within a population may be maintained by balancing selection if different values of personality traits are favoured under different conditions. We measured personality in 98 female North American red squirrels ( Tamiasciurus hudsonicus Erxleben), and examined whether its variation could be maintained by changing selection pressures acting via reproductive traits and yearly variation in food abundance. There was no effect of personality on parturition date or litter size, but a female's activity was correlated to the growth rate of her offspring in the nest, and her aggressiveness was correlated to their survival in the nest and overwinter. The magnitude and direction of the effects changed among life history stages and years, possibly in association with food supply in some cases, and may indicate a role for balancing selection in the maintenance of personality.     

Selection on offspring size varies within and among families in relation to host nutritional quality

Life history theory often assumes a positive relationship between offspring size and fitness, although the strength and form of this relationship is expected to vary with environmental conditions. In arthropods, surprisingly few studies have examined the influence of larval environment on the offspring size–fitness relation. In phytophagous insects, the few studies that have examined variation in larval host plants have found a negative correlation between host plant nutritional quality and the strength of selection favoring larger offspring size, suggesting that this pattern might be general. I present experimental evidence for such a relationship in a population of the moth Rothschildia lebeau feeding on its three primary host plant species. Unlike previous studies, I consider the effect of offspring size on growth and survival at two levels, both among families and among siblings within families. Neonate caterpillar mass had a significant effect on growth and survival. The effect on growth, however, was weak, resulted primarily from variation among families, and did not differ among host plant diets. The effect on survival was stronger and varied among host plant diets, among families, and within families on different host plants in a manner that was generally consistent with the hypothesized negative correlation between host plant nutritional quality and the strength of selection favoring larger offspring size. Overall, results suggest that the consequences of variation in offspring size for survival within and among families are host plant-dependent in this system.     

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.     

Experimental evidence for adaptive personalities in a wild passerine bird

Individuals of the same species differ consistently in risky actions. Such ‘animal personality’ variation is intriguing because behavioural flexibility is often assumed to be the norm. Recent theory predicts that between-individual differences in propensity to take risks should evolve if individuals differ in future fitness expectations: individuals with high long-term fitness expectations (i.e. that have much to lose) should behave consistently more cautious than individuals with lower expectations. Consequently, any manipulation of future fitness expectations should result in within-individual changes in risky behaviour in the direction predicted by this adaptive theory. We tested this prediction and confirmed experimentally that individuals indeed adjust their ‘exploration behaviour’, a proxy for risk-taking behaviour, to their future fitness expectations. We show for wild great tits (Parus major) that individuals with experimentally decreased survival probability become faster explorers (i.e. increase risk-taking behaviour) compared to individuals with increased survival probability. We also show, using quantitative genetics approaches, that non-genetic effects (i.e. permanent environment effects) underpin adaptive personality variation in this species. This study thereby confirms a key prediction of adaptive personality theory based on life-history trade-offs, and implies that selection may indeed favour the evolution of personalities in situations where individuals differ in future fitness expectations.     

Sexual dimorphism is associated with population fitness in the seed beetle Callosobruchus maculatus

The population consequences of sexual selection remain empirically unexplored. Comparative studies, involving extinction risk, have yielded different results as to the effect of sexual selection on population densities make contrasting predictions. Here, we investigate the relationship between sexual dimorphism (SD) and population productivity in the seed beetle Callosobruchus maculatus, using 13 populations that have evolved in isolation. Geometric morphometric methods and image analysis are employed to form integrative measures of sexual dimorphism, composed of variation in weight, size, body shape, and pigmentation. We found a positive relationship between SD and adult fitness (net adult offspring production) across our study populations, but failed to find any association between SD and juvenile fitness (egg-to-adult survival). Several mechanisms may have contributed to the pattern found, and variance in sexual selection regimes across populations, either in female choice for "good genes" or in the magnitude of direct benefits provided by their mates, would tend to produce the pattern seen. However, our results suggest that evolutionary constraints in the form of intralocus sexual conflict may have been the major generator of the relationship seen between SD and population fitness.