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.     

Adaptive strategies for managing uncertainty may explain personality‐related differences in behavioural plasticity

There is growing evidence that individuals within populations show consistent differences in their behaviour across contexts (personality), and that personality is associated with the extent to which individuals adjust their behaviour as function of changing conditions (behavioural plasticity). We propose an evolutionary explanation for a link between personality and plasticity based upon how individuals manage uncertainty. Individuals can employ three categories of tactics to manage uncertainty. They can 1) gather information (sample) to reduce uncertainty, 2) show strategic (state‐dependent) preferences for options that differ in their associated variances in rewards (i.e. variance‐sensitivity), or 3) invest in insurance to mitigate the consequences of uncertainty. We explicitly outline how individual differences in the use of any of these tactics can generate personality‐related differences in behavioural plasticity. For example, sampling effort is likely to co‐vary with individual activity and exploration behaviours, while simultaneously creating population variation in reactions to changes in environmental conditions. Individual differences in the use of insurance may be associated with differences in risk‐taking behaviours, such as boldness in the face of predation, thereby influencing the degree of adaptive plasticity across individuals. Population variation in responsiveness to environmental changes may also reflect individual differences in variance‐sensitivity, because stochastic change in the environment increases variances in rewards, which may both attract and benefit variance‐prone individuals, but not variance‐averse individuals. We review the existing evidence that individual variation in strategies for managing uncertainty exist, and describe how positive‐feedbacks between sampling, variance‐sensitivity and insurance can maintain and exaggerate even small initial differences between individuals in the relative use of these tactics. Given the pervasiveness of the problem of uncertainty, alternative strategies for managing uncertainty may provide a powerful explanation for consistent differences in behaviour and behavioural plasticity for a wide range of traits.     

What's your move? Movement as a link between personality and spatial dynamics in animal populations

Recent studies have established the ecological and evolutionary importance of animal personalities. Individual differences in movement and space‐use, fundamental to many personality traits (e.g. activity, boldness and exploratory behaviour) have been documented across many species and contexts, for instance personality‐dependent dispersal syndromes. Yet, insights from the concurrently developing movement ecology paradigm are rarely considered and recent evidence for other personality‐dependent movements and space‐use lack a general unifying framework. We propose a conceptual framework for personality‐dependent spatial ecology. We link expectations derived from the movement ecology paradigm with behavioural reaction‐norms to offer specific predictions on the interactions between environmental factors, such as resource distribution or landscape structure, and intrinsic behavioural variation. We consider how environmental heterogeneity and individual consistency in movements that carry‐over across spatial scales can lead to personality‐dependent: (1) foraging search performance; (2) habitat preference; (3) home range utilization patterns; (4) social network structure and (5) emergence of assortative population structure with spatial clusters of personalities. We support our conceptual model with spatially explicit simulations of behavioural variation in space‐use, demonstrating the emergence of complex population‐level patterns from differences in simple individual‐level behaviours. Consideration of consistent individual variation in space‐use will facilitate mechanistic understanding of processes that drive social, spatial, ecological and evolutionary dynamics in heterogeneous environments.     

Innovation as part of a wider behavioural syndrome in the guppy: The effect of sex and body size

Recent work on animal personalities has shown that individuals within populations often differ consistently in various types of behaviour and that many of these behaviours correlate among individuals to form behavioural syndromes. Individuals of certain species have also been shown to differ in their rate of behavioural innovation in arriving at novel solutions to new and existing problems (e.g., mazes, novel foods). Here, we investigate whether behaviours traditionally studied in personality research are correlated with individual rates of innovation as part of a wider behavioural syndrome. Guppies (Poecilia reticulata) of both sexes from three different wild population sources were assessed: (a) exploration of an open area; (b) speed through a three‐dimensional maze; (c) investigation of a novel object; and (d) attraction to a novel food. The covariance structure (syndrome structure) was examined using structural equation modelling. The best model separated behaviours relating to activity in all contexts from rates of exploration/investigation and innovation. Innovative behaviour (utilizing new food and moving through a novel area) in these fish therefore forms part of the same syndrome as the traditional shy‐bold continuum (exploration of an open area and investigation of a novel object) found in many animal personality studies. There were no clear differences in innovation or syndrome structure between the sexes, or between the three different populations. However, body size was implicated as part of the behavioural syndrome structure, and because body size is highly correlated with age in guppies, this suggests that individual behavioural differences in personality/innovation in guppies may largely be driven by developmental state.     

Lifetime low behavioural plasticity of personality traits in the common vole (Microtus arvalis) under laboratory conditions

Individual differences in behaviour, referred to as animal personality, are consistent across time and contexts. Nevertheless, personality traits show behavioural plasticity, much like many other phenotypic traits. In the present study, we examined the relationship between personality traits and behavioural plasticity in the common vole (Microtus arvalis) under stable, long-lasting laboratory conditions. A total of 94 voles were tested in the classic open field test, designed to measure seven behavioural parameters (distance moved, grooming, immobility, rearing, running, scanning and walking duration) during a three-minute test. A total of 60 voles formed the experimental group and were tested at four different time points over their lifetime (1st, 3rd, 5th and 7th month); 34 voles formed the control group and were tested only once at the 7th month. All voles were of the same age. Based on principal component analysis (PCA), two ordination axes were determined: “exploration” and “activity.” For further analyses, “distance moved” and “scanning duration” were selected from the first axis and “walking duration” from the second. Using linear mixed-effect models (LMMs), we found highly significant random intercepts (i.e. personality traits) in all three behavioural parameters. However, evidence for behavioural plasticity was only found in the distance moved parameter, as determined from the random slope, and correlations between personality trait (intercept) and plasticity (slope) were not significant for any trait. During the experiment, variances of random effects were high and remained essentially the same, whilst the rank order of many individuals changed. Based on fixed effect slopes and a comparison with the control group, habituation was only significant for “walking duration.” The observed low behavioural plasticity could mirror stable (laboratory) conditions that result in the manifestation of original trait settings (genetic, early postnatal) or their gradual overcoming. These findings provide a starting point for further tests on free-living voles.     

Population differences in behaviour are explained by shared within‐population trait correlations

Correlations in behavioural traits across time, situation and ecological context (i.e. ‘behavioural syndromes’ or ‘personality’) have been documented for a variety of behaviours, and in diverse taxa. Perhaps the most controversial inference from the behavioural syndromes literature is that correlated behaviour may act as an evolutionary constraint and evolutionary change in one’s behaviour may necessarily involve shifts in others. We test the two predictions of this hypothesis using comparative data from eighteen populations of the socially polymorphic spider, Anelosimus studiosus (Araneae, Theriidae). First, we ask whether geographically distant populations share a common syndrome. Second, we test whether population differences in behaviour are correlated similarly to within‐population trait correlations. Our results reveal that populations separated by as much as 36° latitude shared similar syndromes. Furthermore, population differences in behaviour were correlated in the same manner as within‐population trait correlations. That is, population divergence tended to be along the same axes as within‐population covariance. Together, these results suggest a lack of evolutionary independence in the syndrome’s constituent traits.     

Express your personality or go along with the group: what determines the behaviour of shoaling perch?

Behavioural syndromes, defined as correlated behaviours in different contexts, have been studied across species and taxa including humans as part of a personality concept. While most studies have focused on solitary individuals, less is known on how shoaling fish compromise between own personality and group behaviour. Risk-taking behaviour in 1-year-old perch (Perca fluviatilis) was observed to compare individual behaviour when in a group and when alone. An experimental design gave the fish the choice between foraging in an open area in the presence of a piscivore and hiding in the vegetation. We quantified the variation accountable by the effect of individuals being in a group, individuals alone and repeated measurements, using hierarchical mixed effects models. Within-group variances were low, but when individuals were later tested alone, individual differences explained most of the variation. Still, the individual best linear unbiased predictors (BLUPs) of time spent in the open area, extracted from the random effects of the mixed effects model, were positively correlated with the corresponding BLUPs when alone. The results indicate that individual behavioural traits are to some degree expressed also within groups. Most fish showed a shyer behaviour when alone, but bolder individuals changed less between treatments than did shyer ones, suggesting a more influential role of bold fish in the group.     

Sex and the Syndrome: Individual and Population Consistency in Behaviour in Rock Pool Prawn Palaemon elegans

Animal personality has been widely documented across a range of species. The concept of personality is composed of individual behavioural consistency across time and between situations, and also behavioural trait correlations known as behavioural syndromes. Whilst many studies have now investigated the stability of individual personality traits, few have analysed the stability over time of entire behavioural syndromes. Here we present data from a behavioural study of rock pool prawns. We show that prawns are temporally consistent in a range of behaviours, including activity, exploration and boldness, and also that a behavioural syndrome is evident in this population. We find correlations between many behavioural traits (activity, boldness, shoaling and exploration). In addition, behavioural syndrome structure was consistent over time. Finally, few studies have explicitly studied the role of sex differences in personality traits, behavioural consistency and syndrome structure. We report behavioural differences between male and female prawns but no differences in patterns of consistency. Our study adds to the growing literature on animal personality, and provides evidence showing that syndromes themselves can exhibit temporal consistency.     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity?

Human‐altered environmental conditions affect many species at the global scale. An extreme form of anthropogenic alteration is the existence and rapid increase of urban areas. A key question, then, is how species cope with urbanization. It has been suggested that rural and urban conspecifics show differences in behaviour and personality. However, (i) a generalization of this phenomenon has never been made; and (ii) it is still unclear whether differences in personality traits between rural and urban conspecifics are the result of phenotypic plasticity or of intrinsic differences. In a literature review, we show that behavioural differences between rural and urban conspecifics are common and taxonomically widespread among animals, suggesting a significant ecological impact of urbanization on animal behaviour. In order to gain insight into the mechanisms leading to behavioural differences in urban individuals, we hand‐raised and kept European blackbirds (Turdus merula) from a rural and a nearby urban area under common‐garden conditions. Using these birds, we investigated individual variation in two behavioural responses to the presence of novel objects: approach to an object in a familiar area (here defined as neophilia), and avoidance of an object in a familiar foraging context (defined as neophobia). Neophilic and neophobic behaviours were mildly correlated and repeatable even across a time period of one year, indicating stable individual behavioural strategies. Blackbirds from the urban population were more neophobic and seasonally less neophilic than blackbirds from the nearby rural area. These intrinsic differences in personality traits are likely the result of microevolutionary changes, although we cannot fully exclude early developmental influences.     

Singing Activity Reveals Personality Traits in Great Tits

In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well‐studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.     

A mechanistic theory of personality‐dependent movement behaviour based on dynamic energy budgets

Consistent between‐individual differences in movement are widely recognised across taxa. In addition, foraging plasticity at the within‐individual level suggests a behavioural dependency on the internal energy demand. Because behaviour co‐varies with fast‐slow life history (LH) strategies in an adaptive context, as theoretically predicted by the pace‐of‐life syndrome hypothesis, mass/energy fluxes should link behaviour and its plasticity with physiology at both between‐ and within‐individual levels. However, a mechanistic framework driving these links in a fluctuating ecological context is lacking. Focusing on home range behaviour, we propose a novel behavioural‐bioenergetics theoretical model to address such complexities at the individual level based on energy balance. We propose explicit mechanistic links between behaviour, physiology/metabolism and LH by merging two well‐founded theories, the movement ecology paradigm and the dynamic energetic budget theory. Overall, our behavioural‐bioenergetics model integrates the mechanisms explaining how (1) behavioural between‐ and within‐individual variabilities connect with internal state variable dynamics, (2) physiology and behaviour are explicitly interconnected by mass/energy fluxes, and (3) different LHs may arise from both behavioural and physiological variabilities in a given ecological context. Our novel theoretical model reveals encouraging opportunities for empiricists and theoreticians to delve into the eco‐evolutionary processes that favour or hinder the development of between‐individual differences in behaviour and the evolution of personality‐dependent movement syndromes.     

Behavioural Flexibility and Personality in Zebra Finches

Consistent individual differences in behaviour of animals, that is, personalities, are both widespread and widely studied, but very few studies also include cognitive traits in this context. Animal personality has recently been integrated into the pace‐of‐life‐syndrome hypothesis, relating individual behavioural traits to life history. Variation in cognitive traits could be explained well by this theoretical framework. A risk‐reward trade‐off might lead to different cognitive types: Active birds that learn fast, take risks and probably have a fast lifestyle and less active, slow learning birds that are risk averse but thereby perform better in reversal learning as they probably pay more attention to external cues. We investigated the performance of zebra finches (Taeniopygia guttata) in a cognitively challenging reversal learning task and linked this to two personality traits: activity and fearfulness. Male birds were better in reversal learning than females. While no personality‐related differences occurred in the initial learning of our task, more active and fearful birds relearned the cue–reward association faster. While birds of different sex might have revealed different risk‐taking strategies in the training, our findings do not reveal the expected direction of a risk‐reward trade‐off in the reversal learning. It seems likely that a more general and personality‐related cognitive ability might improve performance across different tasks. The linkage between personality and cognition documented here could hence suggest that cognitive traits are indeed part of an overall pace‐of‐life syndrome.     

Evolutionary Perspective on the Interplay Between Family Life,and Parent and Offspring Personality

Consistent inter‐individual variation in behaviour over time and across contexts has been reported for a wide variety of animals, a phenomenon commonly referred to as personality. As behavioural patterns develop inside families, rearing conditions could have lasting effects on the expression of adult personality. In species with parental care, conflicts among family members impose selection on parental and offspring behaviour through coadaptation. Here, we argue that the interplay between the evolution of personality traits (i.e. boldness, exploration, activity, aggressiveness and sociability) expressed outside the family context and the specialized behaviours expressed inside families (i.e. offspring begging behaviour and parental response to offspring solicitations) can have important evolutionary consequences. Personality differences between parents may relate to the typically observed variation in the way they respond to offspring demand, and dependent offspring may already express personality differences, which may relate to the way they communicate with their parents and siblings. However, there has been little research on how personality relates to parental and offspring behaviours. Future research should thus focus on how and why personality may be related to the specialized parent and offspring behaviour that evolved as adaptations to family life.     

Variation in Helper Type Affects Group Stability and Reproductive Decisions in a Cooperative Breeder

Recent studies have shown that differences in life history may lead to consistent inter‐individual variation in behavioural traits, so‐called behavioural syndromes, animal personalities or temperaments. Consistencies of behaviours and behavioural syndromes have mainly been studied in non‐cooperative species. Insights on the evolution of cooperation could be gained from studying individual differences in life histories and behavioural traits. Kin selection theory predicts that if an individual’s reproductive ability is low, it had to aim at gaining inclusive fitness benefits by helping others. We tested this prediction in the cooperatively breeding cichlid Neolamprologus pulcher, by assessing reproductive parameters of adults that had been tested earlier for aggressiveness and for their propensity to assist breeders when they had been young (‘juveniles’). We found that juvenile aggression levels predicted the acceptance of a subordinate in the group when adult. Males which were aggressive as juveniles were significantly more likely to tolerate a subordinate in the group when compared with males which were peaceful as juveniles, whereas females which were more aggressive as juveniles tended to expel subordinates more often. Females produced significantly smaller clutches when paired to males which had helped more as a juvenile, despite the fact that adult males hardly provided direct brood care. There was no evidence that females with a high propensity to help when young, produced smaller clutches or eggs when adult, but they took longer to lay their first clutch when compared with females with a low propensity to help when young. These results suggest that variation in behavioural types might explain variation in cooperation, the extent of group‐living and reproductive decisions.     

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.     

Urine marking in male common voles: Does behavioural activity matter?

Rodent urine provides animals with a large amount of information, from the identity of the animal through its physical condition to social status. Many studies therefore focus on rodent urine-marking behaviour and use marking frequency as an indicator of social status or competitive ability. However, marking, like many other aspects of rodent behaviour, may be affected by individual behavioural activity, a factor that has not been examined so far. We therefore studied a relationship between male urine-marking in reaction to another male's marks (standard opponent) and individual personality profile, characterised by behavioural activity in an open field test (OFT). The marking appeared to be consistent and specific for particular individuals as there was a significant positive relationship between individual markings in two different phases of the experiment. The linkage between behavioural activity in the OFT and urine-marking frequency was non-linear (quadratic), which suggested that males with intermediate activity marked more intensively than males from the extremes of the behavioural spectra. The relationship between the opponent's and the tested males' markings was positive, however, we found no statistically significant evidence that the voles would attempt to overmark the opponent. Marking thus seems to have more of a self-advertising than a competitive function in the common vole. Further, as high marking activity is under strong intra- or intersexual selection, the result might suggest a stabilising selection of the personality trait described as behavioural activity in our study.     

Within‐Individual Correlations Reveal Link Between a Behavioral Syndrome,Condition, and Cortisol in Free‐Ranging Belding's Ground Squirrels

Animals often exhibit consistent individual differences in behavior (i.e., animal personality) and correlations between behaviors (i.e., behavioral syndromes), yet the causes of those patterns of behavioral variation remain insufficiently understood. Many authors hypothesize that state‐dependent behavior produces animal personality and behavioral syndromes. However, empirical studies assessing patterns of covariation among behavioral traits and state variables have produced mixed results. New statistical methods that partition correlations into between‐individual and residual within‐individual correlations offer an opportunity to more sufficiently quantify relationships among behaviors and state variables to assess hypotheses of animal personality and behavioral syndromes. In a population of wild Belding's ground squirrels (Urocitellus beldingi), we repeatedly measured activity, exploration, and response to restraint behaviors alongside glucocorticoids and nutritional condition. We used multivariate mixed models to determine whether between‐individual or within‐individual correlations drive phenotypic relationships among traits. Squirrels had consistent individual differences for all five traits. At the between‐individual level, activity and exploration were positively correlated whereas both traits negatively correlated with response to restraint, demonstrating a behavioral syndrome. At the within‐individual level, condition negatively correlated with cortisol, activity, and exploration. Importantly, this indicates that although behavior is state‐dependent, which may play a role in animal personality and behavioral syndromes, feedback mechanisms between condition and behavior appear not to produce consistent individual differences in behavior and correlations between them.     

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.     

Behaviour in captivity predicts some aspects of natural behaviour,but not others,in a wild cricket population

Examining the relevance of ‘animal personality’ involves linking consistent among- and within-individual behavioural variation to fitness in the wild. Studies aiming to do this typically assay personality in captivity and rely on the assumption that measures of traits in the laboratory reflect their expression in nature. We examined this rarely tested assumption by comparing laboratory and field measurements of the behaviour of wild field crickets (Gryllus campestris) by continuously monitoring individual behaviour in nature, and repeatedly capturing the same individuals and measuring their behaviour in captivity. We focused on three traits that are frequently examined in personality studies: shyness, activity and exploration. All of them showed repeatability in the laboratory. Laboratory activity and exploration predicted the expression of their equivalent behaviours in the wild, but shyness did not. Traits in the wild were predictably influenced by environmental factors such as temperature and sunlight, but only activity showed appreciable within-individual repeatability. This suggests that some behaviours typically studied as personality traits can be accurately assayed in captivity, but the expression of others may be highly context-specific. Our results highlight the importance of validating the relevance of laboratory behavioural assays to analogous traits measured in the wild.