Animal personality

Consistent individual differences in parenting are widespread; however, we know little about why there is variation in parenting behavior among individuals within species. One possible explanation for consistent individual differences in parenting is that individuals invest in different aspects of parental care, such as provisioning or defense. In this field study we measured consistent individual differences in parenting behavior and evaluated correlations between parenting and other behaviors in threespine stickleback (Gasterosteus aculeatus). We repeatedly measured male parenting behavior and male behavior in the presence of three different types of live intruders: a female, a conspecific male, and a predator, meant to provoke courtship, aggressive and antipredator behavior, respectively. While males plastically adjusted their reactions to different types of intruders, we found consistent individual differences in behavior (behavioral types) both within and across contexts, even after accounting for variation in body size and nest characteristics. Males that performed more parenting behavior responded faster to all types of intruders. These results suggest that in nature, individual male stickleback exhibit robust parental behavioral types, and highly parental males are more attentive to their surroundings. Future studies are needed to examine the potential causes of individual variation in parental behavior in the field.

Resting metabolic rate (RMR) is highly variable between individuals within a single species and the relationship between body mass and RMR does not wholly explain this variability. One factor that could account for a portion of the residual variation is animal personality or consistent individual differences (CIDs) in behaviour, but no study has examined this relationship in a free-living population of mammals. In this paper, we test for a relationship between RMR and CIDs in activity in live-trapped meadow voles Microtus pennsylvanicus after controlling for the effect of body mass. We quantified the activity levels of voles both in an unfamiliar environment and for the first 2 min in the metabolic apparatus, and then measured RMR using open-flow respirometry. As expected, there was a linear relationship between RMR and body mass, and we found strong evidence for repeatable differences in activity levels between individuals. However, contrary to the hypothesis, we did not identify a significant correlation between CIDs in behaviour and RMR after controlling for body mass. Our results suggest that, at least within species, higher activity levels may not require a greater investment in energetically demanding tissues or increased capacity for processing of energy. Alternatively, if a relationship exists, our inability to detect it may reflect a weak behavioural signal in noisy RMR data that are influenced by many factors. Our results could also reflect an artefact of individual responses to stress or a sampling bias towards more exploratory individuals in animals captured by live-trapping.

The existence of personalities has been explored in various invertebrates, but a comprehensive investigation of personality differences across individuals in a eusocial insect has not yet been conducted. The study of personality differences across individuals within the same behavioral caste may contribute to an understanding of how social insects divide labor within the nest. Here, we define and investigate three dimensions of personality within the worker caste of a model social insect, the honey bee Apis mellifera, as follows: (1) consistent individual behavioral differences over time, (2) consistent individual behavioral differences across contexts, and (3) the presence of correlated suites of behaviors. To test whether honey bee workers exhibit dimensions 1 and 2, we repeatedly assessed responses of groups of same-age bees in cages to stimuli that are relevant to bee life history. To test for dimension 3, we examined behavior within a colony context by using observation hives to record the behaviors of individual bees across their lifetimes. Our results provide some evidence for all three dimensions of personality in honey bee workers. In particular, our data suggest some individuals may be more likely to be highly interactive with other workers (e.g., engaging in food sharing), while other individuals are consistently less interactive. These findings expand upon and contribute to previous models for the organization of worker division of labor in honey bees, suggesting that consistent behavioral differences (personalities) of workers within a behavioral caste have the potential to contribute to subcaste division of labor. Behavioral ecologists have become increasingly interested in animal personalities, individual behavioral differences that are consistent over time and in different contexts, with recent focus on understanding the occurrence of personalities across taxa and their adaptive value. The existence and function of personality differences among individuals in complex societies, such as eusocial insects, remain understudied. Here, we provide the first comprehensive investigation of whether workers of the highly eusocial honey bee show hallmarks of personality. Although these workers demonstrate well-documented behavioral changes as they age, we uncovered some aspects of their behavior, in particular, their tendency to physically interact with other bees, remain somewhat consistent even as they age and change roles within the colony. We suggest that individual-level personality differences have the potential to contribute to colony division of labor by creating variation in individual tendencies to perform different tasks.

Despite increasing interest, animal personality is still a puzzling phenomenon. Several theoretical models have been proposed to explain intraindividual consistency and interindividual variation in behaviour, which have been primarily supported by qualitative data and simulations. Using an empirical approach, I tested predictions of one main life-history hypothesis, which posits that consistent individual differences in behaviour are favoured by a trade-off between current and future reproduction. Data on life-history were collected for individuals of a natural population of grey mouse lemurs (Microcebus murinus). Using open-field and novel-object tests, I quantified variation in activity, exploration and boldness for 117 individuals over 3 years. I found systematic variation in boldness between individuals of different residual reproductive value. Young males with low current but high expected future fitness were less bold than older males with high current fecundity, and males might increase in boldness with age. Females have low variation in assets and in boldness with age. Body condition was not related to boldness and only explained marginal variation in exploration. Overall, these data indicate that a trade-off between current and future reproduction might maintain personality variation in mouse lemurs, and thus provide empirical support of this life-history trade-off hypothesis.

Consistent individual differences in behaviour, and behavioural correlations within and across contexts, are referred to as animal personalities. These patterns of variation have been identified in many animal taxa and are likely to have important ecological and evolutionary consequences. Despite their importance, genetic and environmental sources of variation in personalities have rarely been characterized in wild populations. We used a Bayesian animal model approach to estimate genetic parameters for aggression, activity and docility in North American red squirrels (Tamiasciurus hudsonicus). We found support for low heritabilities (0.08-0.12), and cohort effects (0.07-0.09), as well as low to moderate maternal effects (0.07-0.15) and permanent environmental effects (0.08-0.16). Finally, we found evidence of a substantial positive genetic correlation (0.68) and maternal effects correlation (0.58) between activity and aggression providing evidence of genetically based behavioural correlations in red squirrels. These results provide evidence for the presence of heritable variation in red squirrel behaviour, but also emphasize the role of other sources of variation, including maternal effects, in shaping patterns of variation and covariation in behavioural traits.

The origins of consistent individual differences in cooperation in wild banded mongooses, Mungos mungo

Although individual differences in the behavior of animals, sometimes referred to as personality, have recently received considerable attention, the development of such differences remains understudied. We previously found consistent individual differences in behavior in four tests simulating everyday contexts in 74 preweaning age kittens from 16 litters of the domestic cat. To study the development of consistent among-individual differences in four behavioral traits in cats, we followed a subset of these same individuals and repeated the same tests at 6 and 12 months of age. Some individual differences in behavior became increasingly repeatable with age due to a combination of decreased individual-level variance (canalization) and increased among-individual variance; these changes in variance and repeatability continued into adulthood (12 months). We did not observe behavioral syndromes at any age, in contrast to our previous reports in a different population of adult cats. The mechanisms that underlie increased repeatability with age and the possibility of personality structure differing between populations in this species remain to be studied.

The past decade has seen an extraordinary rise in the number of papers devoted to the study of consistent individual differences in behavior, termed variably as types, temperament, correlated phenotypes, and/or syndromes. In earnest, the acceleration of this field was initiated by a handful of reviews that focused on the ecological and evolutionary implications of personality, published in 2004(Dall et al., 2004; Sih et al., 2004a; Sih et al., 2004b). Although, the literature on animal personality had already experienced a rich history in the comparative psychology literature by this time (Gosling and John, 1999; Gosling, 2001). Earlier works by Felicity Huntingford (Huntingford, 1976) and Susan Riechert (Riechert and Hedrick, 1993; Riechert et al., 2001), along with more contemporary studies by Niels Dingemanse (Dingemanse et al., 2002; Dingemanse et al., 2003), had each hinted at the ecological significance of animal personalities for years. However, it was this synthesis of these case studies into a unified framework by Andy Sih and others that lead to the field's meteoric rise. The field of animal personality became enormously popular in the years following these early reviews. Hundreds of papers were published from countless study systems, e.g., birds , lizards (Cote et al., 2008; Carter et al., 2010), fish (Bell, 2005; Biro et al., 2010), squid (Sinn et al., 2008; Sinn et al., 2010), small mammals (Dochtermann and Jenkins, 2007), spiders (Johnson and Sih, 2005; Pruitt et al., 2008; Sweeney et al., 2013), crickets (Wilson et al., 2010). These studies tended to focus on documenting the presence of behavioral consistency and describing the correlations observed in behavioral measures across multiple ecological contexts. Traits like activity level, boldness, and aggressiveness were among the most commonly measured traits(Sih and Bell, 2008). However, at the same time as this rise in popularity, the field of animal personality was also bombarded with skepticism. In particular, many investigators questioned the true novelty of the animal personality movement, whether it would have tenure, and whether the animal personality perspective could be used profitably as an organization framework for the study of the long-standing goals/questions in behavior, ecology, and evolution. So, the field of animal personality deepened and diversified. Between the years of 2009 and 2014, dozens of reviews, ideas and perspectives pieces emerged (e.g., Cote et al., 2010; Stamps and Groothuis, 2010; Sih et al., 2012; Jandt et al., 2013). They considered various subsets of the emerging literature, and convincingly argued the potential implications of personality for fields ranging from behavioral genomics, to species interactions, invasion biology, sexual selection, epidemiology, and animal welfare, among others. These reviews, in turn, rapidly received dozens or hundreds of citations themselves and the number of plausible implications of animal personality grew to be truly overwhelming. Now, at least in my own view, the challenge for the field is to harness these ideas and test their utility in situ.

Consistent individual differences in behaviour, or ‘personality’, are likely to be influenced by development, social context, and species ecology, though few comparative, longitudinal studies exist. Here, we investigated the role of development and social context on personality variation in two identically reared, social corvids: common ravens and carrion crows. We repeatedly presented subjects with a variety of novel food and objects, while alone and in a primarily sibling subgroup, from fledging to sub-adulthood. We predicted that consistent individual differences would emerge later in development, and that conspecific presence would facilitate behavioural similarities. In contrast to our predictions, we found that individuals of both species were highly inconsistent in their behavioural responses throughout the development period. In line with our predictions, though in the ravens only, conspecific presence promoted behavioural similarities as individuals were strongly shaped by their subgroup, and it is likely that these effects were driven by social context rather than relatedness. We discuss these findings in relation to developmental steps and the role of social relations in these species. Overall, our findings highlight that these two species are highly adaptable in their behaviour, and the ravens in particular are strongly influenced by their social environment, which may facilitate cooperation and social learning.

Sampling bias resulting from animal personality

Research on consistent individual differences in behavior, or “behavioral syndromes”, continues to grow rapidly, and yet, the aspects of behavior under consideration have remained remarkably limited. Here, we consider individual variation in consistency of choice (termed here “choosiness”), as expressed during habitat choice. We repeatedly tested the responses of female Western Black Widows, Latrodectus hesperus, to two cues of habitat quality: prey chemical cues and variation in web site illuminance. We estimated females’ response by the distance they positioned themselves from (1) the source of prey chemical cues and (2) the darkest edge of our test arena. Individuals with low variance in their responses are deemed more “choosy”, whereas individuals with high variance are deemed less “choosy”. Generally, most females initiated web construction near the source of the prey chemical cues and tended to place themselves in low-light conditions. However, we detected strong, repeatable differences in females’ intensity of response, and within-individual variance of response (i.e., choosiness) was correlated across situations: females with highly consistent responses towards cricket chemical cues also exhibited highly consistent responses towards variation in light conditions. When deprived of food for extended periods, females were indistinguishable in their responses towards prey chemical cues, but tended to initiate web construction in brighter lighting conditions. Food-deprived females universally exhibited higher variance and diminished consistency in their responses (i.e., they were less choosy). Additionally, higher choosiness was associated with greater mass loss during choice trials, suggesting choosiness is energetically costly. Our results demonstrate that consistency of response to environmental cues is yet another element of behavior that varies among individuals and variation in choosiness could beget speed/quality trade-offs during animal decision making.

Chimpanzees have consistent individual differences in behaviour, also referred to as personality. Similar to human personality structure, five dimensions are commonly found in chimpanzee studies that show evidence for convergent and predictive validity (Dominance, Openness, Extraversion, Agreeableness, and Reactivity/Undependability). These dimensions are to some extent heritable, indicating a genetic component that explains part of the variation in personality scores, but are also influenced by environmental factors, such as the early social rearing background of the individuals. In this study, we investigated the role of epigenetic modification of the dopamine receptor D2 gene (DRD2) as a potential mechanism underlying personality variation in 51 captive chimpanzees. We used previously collected personality trait rating data and determined levels of DRD2 CpG methylation in peripheral blood samples for these same individuals. Results showed that DRD2 methylation is most strongly associated with Extraversion, and that varying methylation levels at specific DRD2 sites are associated with changes in Extraversion in nursery-reared, but not mother-reared, individuals. These results highlight the role of dopaminergic signalling in chimpanzee personality, and indicate that environmental factors, such as social experiences early in life, can have long-lasting behavioural effects, potentially through modification of the epigenome. These findings add to the growing evidence demonstrating the importance of the experience-dependent methylome for the development of complex social traits like personality.

Individuals respond differently to stressors and it has been suggested that stress responses are related to coping styles (consistent individual differences in behavior and physiology). We studied behavioral responses to a novel object and corticosterone response to stress during chick rearing in free-living female house sparrows (Passer domesticus). To prevent mates from influencing each others' behavior, we removed the males temporarily from nests and tested the females the following day either with a novel object placed on the nest box or as control. The two groups differed only in behaviors that were a priori defined as responses to the novel object (latency to first feeding, time spent near the nest, and inspecting the novel object by hovering in front of it) indicating that mate-removal per se had no effect on female behavior. Based on these variables, females' coping behaviors were categorized as 'bold', 'inquisitive' or 'shy' by discriminant analysis. Baseline corticosterone, measured on the day following the novel-object or control test, was not related to any measure of coping. Stress-induced corticosterone, however, was negatively related to number of hoverings in front of the nest (a measure of explorativeness) and accordingly differed between the behavioral coping categories, with 'inquisitive' birds having the lowest stress response. We propose that the relationship between physiological stress response and behavioral response to novelty (a component of personality or coping style) may be more complex than previously suggested, and individuals cannot always be unambiguously categorized along a single personality axis.

Despite the growing evidence for the importance of developmental experiences shaping consistent individual differences in behaviour and physiology, the role of endocrine factors underlying the development and maintenance of such differences across multiple traits, remains poorly understood. Here, we investigated how an experimental manipulation of circulating glucocorticoids during early adolescence affects behavioural and physiological variation and covariation later in life in the precocial cavy (Cavia aperea). Plasma cortisol concentrations were experimentally elevated by administering cortisol via food for 3 weeks. Struggle docility, escape latency, boldness, exploration and social behaviour were then tested three times after individuals attained sexual maturity. In addition, blood samples were taken repeatedly to monitor circulating cortisol concentrations. Exogenous cortisol affected mean trait expression of plasma cortisol levels, struggle docility and escape latency. Repeatability of cortisol and escape latency was increased and repeatability of struggle docility tended to be higher (approaching significance) in treated individuals. Increased repeatability was mainly caused by an increase of among-individual variance. Correlations among docility, escape latency and cortisol were stronger in treated animals compared to control animals. These results suggest that exposure to elevated levels of cortisol during adolescence can alter animal personality traits as well as behavioural syndromes. Social and risk-taking traits showed no correlation with cortisol levels and were unaffected by the experimental manipulation, indicating behavioural modularity. Taken together, our data highlight that cortisol can have organising effects during adolescence on the development of personality traits and behavioural syndromes, adding to the increasing evidence that not only early life but also adolescence is an important sensitive period for behavioural development.

Consistent individual differences in behaviour across time or contexts (i.e. personality types) have been found in many species and have implications for fitness. Likewise, individual variation in cognitive abilities has been shown to impact fitness. Cognition and personality are complex, multidimensional traits. However, previous work has generally examined the connection between a single personality trait and a single cognitive ability, yielding equivocal results. Links between personality and cognitive ability suggest that behavioural traits coevolved and highlight their nuanced connections. Here we examined individuals' performance on multiple personality tests and repeated problem-solving tests (each measuring innovative performance). We assessed behavioural traits (dominance, boldness, activity, risk-taking, aggressiveness and obstinacy) in 41 captive zebra finches. Birds' scores for boldness and obstinacy were consistent over two years. We also examined whether personality correlated with problem-solving performance on repeated tests. Our results indicate that neophobia, dominance and obstinacy were related to successful solving, and less dominant, more obstinate birds solved the tasks quicker on average. Our results indicate the importance of examining multiple measures over a long period. Future work that identifies links between personality and innovation in non-model organisms may elucidate the coevolution of these two forms of individual differences.