Parasitism and the evolutionary ecology of animal personality

The ecological factors responsible for the evolution of individual differences in animal personality (consistent individual differences in the same behaviour across time and contexts) are currently the subject of intense debate. A limited number of ecological factors have been investigated to date, with most attention focusing on the roles of resource competition and predation. We suggest here that parasitism may play a potentially important, but largely overlooked, role in the evolution of animal personalities. We identify two major routes by which parasites might influence the evolution of animal personality. First, because the risk of acquiring parasites can be influenced by an individual's behavioural type, local parasite regimes may impose selection on personality traits and behavioural syndromes (correlations between personality traits). Second, because parasite infections have consequences for aspects of host 'state', parasites might induce the evolution of individual differences in certain types of host behaviour in populations with endemic infections. Also, because infection often leads to specific changes in axes of personality, parasite infections have the potential to decouple behavioural syndromes. Host-parasite systems therefore provide researchers with valuable tools to study personality variation and behavioural syndromes from a proximate and ultimate perspective.     

Individual personalities predict social behaviour in wild networks of great tits (Parus major)

Social environments have an important effect on a range of ecological processes, and form a crucial component of selection. However, little is known of the link between personality, social behaviour and population structure. We combine a well‐understood personality trait with large‐scale social networks in wild songbirds, and show that personality underpins multiple aspects of social organisation. First, we demonstrate a relationship between network centrality and personality with ‘proactive’ (fast‐exploring) individuals associating weakly with greater numbers of conspecifics and moving between flocks. Second, temporal stability of associations relates to personality: ‘reactive’ (slow‐exploring) birds form synergistically stable relationships. Finally, we show that personality influences social structure, with males non‐randomly distributed across groups. These results provide strong evidence that songbirds follow alternative social strategies related to personality. This has implications not only for the causes of social network structure but also for the strength and direction of selection on personality in natural populations.     

Personality-dependent dispersal in the invasive mosquitofish: group composition matters

Understanding/predicting ecological invasions is an important challenge in modern ecology because of their immense economical and ecological costs. Recent studies have revealed that within-species variation in behaviour (i.e. animal personality) can shed light on the invasion process. The general hypothesis is that individuals' personality type may affect their colonization success, suggesting that some individuals might be better invaders than others. We have recently shown that, in the invasive mosquitofish (Gambusia affinis), social personality trait was an important indicator of dispersal distance, with more asocial individuals dispersing further. Here, we tested how mean personality within a population, in addition to individual personality type, affect dispersal and settlement decisions in the mosquitofish. We found that individual dispersal tendencies were influenced by the population's mean boldness and sociability score. For example, individuals from populations with more asocial individuals or with more bold individuals are more likely to disperse regardless of their own personality type. We suggest that identifying behavioural traits facilitating invasions, even at the group level, can thus have direct applications in pest management.     

Social traits,social networks and evolutionary biology

The social environment is both an important agent of selection for most organisms, and an emergent property of their interactions. As an aggregation of interactions among members of a population, the social environment is a product of many sets of relationships and so can be represented as a network or matrix. Social network analysis in animals has focused on why these networks possess the structure they do, and whether individuals’ network traits, representing some aspect of their social phenotype, relate to their fitness. Meanwhile, quantitative geneticists have demonstrated that traits expressed in a social context can depend on the phenotypes and genotypes of interacting partners, leading to influences of the social environment on the traits and fitness of individuals and the evolutionary trajectories of populations. Therefore, both fields are investigating similar topics, yet have arrived at these points relatively independently. We review how these approaches are diverged, and yet how they retain clear parallelism and so strong potential for complementarity. This demonstrates that, despite separate bodies of theory, advances in one might inform the other. Techniques in network analysis for quantifying social phenotypes, and for identifying community structure, should be useful for those studying the relationship between individual behaviour and group‐level phenotypes. Entering social association matrices into quantitative genetic models may also reduce bias in heritability estimates, and allow the estimation of the influence of social connectedness on trait expression. Current methods for measuring natural selection in a social context explicitly account for the fact that a trait is not necessarily the property of a single individual, something the network approaches have not yet considered when relating network metrics to individual fitness. Harnessing evolutionary models that consider traits affected by genes in other individuals (i.e. indirect genetic effects) provides the potential to understand how entire networks of social interactions in populations influence phenotypes and predict how these traits may evolve. By theoretical integration of social network analysis and quantitative genetics, we hope to identify areas of compatibility and incompatibility and to direct research efforts towards the most promising areas. Continuing this synthesis could provide important insights into the evolution of traits expressed in a social context and the evolutionary consequences of complex and nuanced social phenotypes.     

Personality and Affinities Play a Key Role in the Organisation of Collective Movements in a Group of Domestic Horses

Understanding how groups of individuals with different motives come to daily decisions about the exploitation of their environment is a key question in animal behaviour. While interindividual differences are often seen only as a threat to group cohesion, growing evidence shows that they may to some extent facilitate effective collective action. Recent studies suggest that personality differences influence how individuals are attracted to conspecifics and affect their behaviour as an initiator or a follower. However, most of the existing studies are limited to a few taxa, mainly social fish and arthropods. Horses are social herbivores that live in long‐lasting groups and show identifiable personality differences between individuals. We studied a group of 38 individuals living in a 30‐ha hilly pasture. Over 200 h, we sought to identify how far individual differences such as personality and affinity distribution affect the dynamic of their collective movements. First, we report that individuals distribute their relationships according to similar personality and hierarchical rank. This is the first study that demonstrates a positive assortment between unrelated individuals according to personality in a mammal species. Second, we measured individual propensity to initiate and found that bold individuals initiated more often than shy individuals. However, their success in terms of number of followers and joining duration did not depend on their individual characteristics. Moreover, joining process is influenced by social network, with preferred partners following each other and bolder individuals being located more often at the front of the movement. Our results illustrate the importance of taking into account interindividual behavioural differences in studies of social behaviours.     

Social Dominance in a Gregarious Bird is Related to Body Size But not to Standard Personality Assays

The recent growth of research on animal personality could provide new insights into our understanding of sociality and the structure of animal groups. Although simple assays of the type commonly used to study animal personality have been shown to correlate with social aggressiveness in some bird species, conflicting empirical results do not yet make it clear when such assays, typically using isolated individuals, predict behaviour within social groups. We measured aggressiveness in groups of a very gregarious species, the common waxbill (Estrilda astrild), and performed five commonly used behavioural assays on the same individuals: tonic immobility, mirror test, novel object test, open‐field test and a variant of the latter in an enriched environment. We found that larger individuals were more dominant and that differences in aggressiveness were repeatable. None of the traditional behavioural assays were related to aggressiveness or dominance. Standard personality assays may fail to capture individual differences relevant to predict social behaviour, and we discuss biological and methodological explanations for these results, such as social behaviour being in part an emergent property of groups rather than an intrinsic property of individuals, or gregarious species being particularly sensitive to the conditions of standard personality assays that test individuals alone.     

Systems approach to studying animal sociality: individual position versus group organization in dynamic social network models

Social networks can be used to represent group structure as a network of interacting components, and also to quantify both the position of each individual and the global properties of a group. In a series of simulation experiments based on dynamic social networks, we test the prediction that social behaviors that help individuals reach prominence within their social group may conflict with their potential to benefit from their social environment. In addition to cases where individuals were able to benefit from improving both their personal relative importance and group organization, using only simple rules of social affiliation we were able to obtain results in which individuals would face a trade-off between these factors. While selection would favor (or work against) social behaviors that concordantly increase (or decrease, respectively) fitness at both individual and group level, when these factors conflict with each other the eventual selective pressure would depend on the relative returns individuals get from their social environment and their position within it. The presented results highlight the importance of a systems approach to studying animal sociality, in which the effects of social behaviors should be viewed not only through the benefits that those provide to individuals, but also in terms of how they affect broader social environment and how in turn this is reflected back on an individual's fitness.     

Fitness consequences of social network position in a wild population of forked fungus beetles (Bolitotherus cornutus)

Social networks describe the pattern of intraspecific interactions within a population. An individual's position in a social network often is expected to influence its fitness, but only a few studies have examined this relationship in natural populations. We investigated the fitness consequences of network position in a wild beetle population. Copulation success of male beetles positively covaried with strength (a measure of network centrality) and negatively covaried with clustering coefficient (CC) (a measure of cliquishness). Further analysis using mediation path models suggested that the activity level of individuals drove the relationships between strength and fitness almost entirely. In contrast, selection on CC was not explained by individual behaviours. Although our data suggest that social network position can experience strong sexual selection, it is also clear that the relationships between fitness and some network metrics merely reflect variation in individual-level behaviours.     

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.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Initiative, personality and leadership in pairs of foraging fish

Studies of coordinated movement have found that, in many animal species, bolder individuals are more likely to initiate movement and shyer individuals to follow. Here, we show that in pairs of foraging stickleback fish, leadership is not merely a passive consequence of temperamental differences. Instead, the act of initiating a joint foraging trip out of cover itself brings about a change in the role that an individual plays throughout the subsequent trip, and success in recruiting a partner affects an individual's tendency to initiate the next trip. On each joint trip, whichever fish took the initiative in leading out of cover gains greater influence over its partner's behaviour, which persists even after several changes in position (i.e. termination attempts and re-joining). During any given trip, the initiator is less responsive to its partner's movements than during trips initiated by the partner. An individual's personality had an important effect on its response to failure to recruit a partner: while bold fish were unaffected by failures to initiate a joint trip, shy individuals were less likely to attempt another initiation after a failure. This difference provides a positive feedback mechanism that can partially stabilise social roles within the pair, but it is not strong enough to prevent occasional swaps, with individuals dynamically adjusting their responses to one another as they exchange roles.     

Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals

Numerous factors affect the fine-scale social structure of animal groups, but it is unclear how important such factors are in determining how individuals encounter resources. Familiarity affects shoal choice and structure in many social fishes. Here, we show that familiarity between shoal members of sticklebacks (Gasterosteus aculeatus) affects both fine-scale social organization and the discovery of resources. Social network analysis revealed that sticklebacks remained closer to familiar than to unfamiliar individuals within the same shoal. Network-based diffusion analysis revealed that there was a strong untransmitted social effect on patch discovery, with individuals tending to discover a task sooner if a familiar individual from their group had previously done so than if an unfamiliar fish had done so. However, in contrast to the effect of familiarity, the frequency with which individuals had previously associated with one another had no effect upon the likelihood of prey patch discovery. This may have been due to the influence of fish on one another''s movements; the effect of familiarity on discovery of an empty ‘control’ patch was as strong as for discovery of an actual prey patch. Our results demonstrate that factors affecting fine-scale social interactions can also influence how individuals encounter and exploit resources.     

Dominance rank predicts social network position across developmental stages in rhesus monkeys

Social network analysis is increasingly common in studying complex interactions among individuals. Across a range of primates, high-ranking adults are generally more socially connected, which results in better fitness outcomes. However, it still remains unclear whether this relationship between social network position and dominance rank emerges in infancy and whether, in species with a social transmission of dominance rank, social network positions are driven by the presence of the mother. To fill this gap, we first explored whether dominance ranks were related to social network position, measured via eigenvector centrality, in infants, juveniles, and adults in a troop of semi-free-ranging rhesus macaques (Macaca mulatta). We then examined relationships between dominance rank and eigenvector centrality in a peer-only group of yearlings who were reared with their mothers in either a rich, socially complex environment of multigenerational (MG) kin support or a unigenerational group of mothers and their infants from birth through 8 months. In Experiment 1, we found that mother's network position predicted offspring network position and that dominants across all age categories were more central in affiliative networks (social contact, social grooming, and social play). Experiment 2 showed that high-ranking yearlings in a peer-only group were more central only in the social contact network. Moreover, yearlings reared in a socially complex environment of MG kin support were more central. Our findings suggest that the relationship between dominance rank and social network position begins early in life, and that complex early social environments can promote later social competency. Our data add to the growing body of evidence that the presence/absence of the mother and kin influence how dominance rank affects social network position. These findings have important implications for the role of caregivers in the social status of developing primates, which ultimately ties to health and fitness outcomes.     

Information flow through threespine stickleback networks without social transmission

Social networks can result in directed social transmission of learned information, thus influencing how innovations spread through populations. Here we presented shoals of threespine sticklebacks (Gasterosteous aculeatus) with two identical foraging tasks and applied network-based diffusion analysis (NBDA) to determine whether the order in which individuals in a social group contacted and solved the tasks was affected by the group's network structure. We found strong evidence for a social effect on discovery of the foraging tasks with individuals tending to discover a task sooner when others in their group had previously done so, and with the spread of discovery of the foraging tasks influenced by groups' social networks. However, the same patterns of association did not reliably predict spread of solution to the tasks, suggesting that social interactions affected the time at which the tasks were discovered, but not the latency to its solution following discovery. The present analysis, one of the first applications of NBDA to a natural animal system, illustrates how NBDA can lead to insight into the mechanisms supporting behaviour acquisition that more conventional statistical approaches might miss. Importantly, we provide the first compelling evidence that the spread of novel behaviours can result from social learning in the absence of social transmission, a phenomenon that we refer to as an untransmitted social effect on learning.     

Social personalities influence natal dispersal in a lizard

Animal personalities are common across taxa and have important evolutionary and ecological implications. Such consistent individual differences correlate with important life-history traits such as dispersal. Indeed, some environmental conditions are supposed to determine dispersers with a specific personality. For example, an increased density should promote the departure of individuals with less social tolerance. Therefore, we hypothesized that dispersers from high-density populations should primarily be asocial individuals, whereas dispersers from low-density populations should be social individuals. In the common lizard (Lacerta vivipara), we measured attraction towards the odour of conspecifics on juveniles at birth as a metric of social tolerance. We then released these juveniles into populations of different densities and measured dispersal and settlement behaviours with regard to social tolerance. One year later, we again measured the social tolerance of surviving individuals. The social tolerance is constant across time and strongly reflects the individual's dispersal and settlement patterns with respect to population density. These results strongly suggest that social personalities exist and influence dispersal decisions. Further studies will help to elucidate the proximate and ultimate determinants of social personalities.     

Selection for territory acquisition is modulated by social network structure in a wild songbird

The social environment may be a key mediator of selection that operates on animals. In many cases, individuals may experience selection not only as a function of their phenotype, but also as a function of the interaction between their phenotype and the phenotypes of the conspecifics they associate with. For example, when animals settle after dispersal, individuals may benefit from arriving early, but, in many cases, these benefits will be affected by the arrival times of other individuals in their local environment. We integrated a recently described method for calculating assortativity on weighted networks, which is the correlation between an individual's phenotype and that of its associates, into an existing framework for measuring the magnitude of social selection operating on phenotypes. We applied this approach to large‐scale data on social network structure and the timing of arrival into the breeding area over three years. We found that late‐arriving individuals had a reduced probability of breeding. However, the probability of breeding was also influenced by individuals’ social networks. Associating with late‐arriving conspecifics increased the probability of successfully acquiring a breeding territory. Hence, social selection could offset the effects of nonsocial selection. Given parallel theoretical developments of the importance of local network structure on population processes, and increasing data being collected on social networks in free‐living populations, the integration of these concepts could yield significant insights into social evolution.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Social groups with diverse personalities mitigate physiological stress in a songbird

Social groups often consist of diverse phenotypes, including personality types, and this diversity is known to affect the functioning of the group as a whole. Social selection theory proposes that group composition (i.e. social environment) also influences the performance of individual group members. However, the effect of group behavioural composition on group members remains largely unexplored, and it is still contentious whether individuals benefit more in a social environment with homogeneous or diverse behavioural composition. We experimentally formed groups of house sparrows Passer domesticus with high and low diversity of personality (exploratory behaviour), and found that their physiological state (body condition, physiological stress and oxidative damage) improved with increasing group-level diversity of personality. These findings demonstrate that group personality composition affects the condition of group members and individuals benefit from social heterosis (i.e. associating with a diverse set of behavioural types). This aspect of the social life can play a key role in affiliation rules of social animals and might explain the evolutionary coexistence of different personalities in nature.     

Individual‐ and population‐level personalities in a floriphilic katydid

Behaviour, including personality, informs us about the response of animals towards their changing environment. Despite the widespread occurrence of florivorous insects and the important but often underrated ecological roles that they play, the study of florivore behaviour is neglected relative to that of pollinators and other herbivores. Specifically, we do not know how different personality types can develop among florivores and enable them to persist in habitats with an ephemeral and dynamic availability of food resources. To address this knowledge gap, we investigated the following questions: whether the (a) inter‐individual differences of exploration and boldness are consistent; (b) inter‐population differences of exploration and boldness are consistent; (c) exploration and boldness are correlated. We collected individuals of the polyphagous floriphilic katydid, Phaneroptera brevis from four populations from wasteland sites in Singapore and performed a personality assay conducted in an insectary to investigate the exploratory and boldness levels of the individuals and populations. The major novel finding was that the floriphilic P. brevis katydids exhibit population‐level personality types for boldness, but not for exploration. Some katydid individuals were consistently more exploratory and bolder than other individuals. However, contrary to our predictions, we did not find any evidence of behavioural syndromes in the katydid individuals, as the boldness level for individuals was not significantly correlated with exploration for individuals. This suggests that an individual which is more exploratory may not be equally keen to take risks and consume novel food that it encounters. Our findings also suggest that boldness and exploration are linked to ecologically important behaviours, but more studies are needed to better understand population‐level personality and how and why natural selection may favour the evolution of personality in certain populations.