Environmental heterogeneity modifies the link between personality and survival in fluctuating small mammal populations.

Despite numerous studies examining the fitness consequences of animal personalities, predictions concerning the relationship between personality and survival are not consistent with empirical observations. Theory predicts that individuals who are risky (i.e. bold, active and aggressive) should have higher rates of mortality; however, empirical evidence shows high levels of variation in behaviour-survival relationships in wild populations. We suggest that this mismatch between predictions under theory and empirical observations results from environmental contingencies that drive heterogeneity in selection. This uncertainty may constrain any universal directional relationships between personality traits and survival. Specifically, we hypothesize that spatiotemporal fluctuations in perceived risk that arise from variability in refuge abundance and competitor density alter the relationship between personality traits and survival. In a large-scale manipulative experiment, we trapped four small mammal species in five subsequent years across six forest stands treated with different management practices in Maine, United States. Stands all occur within the same experimental forest but contain varying amounts of refuge and small mammal densities fluctuate over time and space. We quantified the effects of habitat structure and competitor density on the relationship between personality traits and survival to assess whether directional relationships differed depending on environmental contingencies. In the two most abundant species, deer mice and southern red-backed voles, risky behaviours (i.e. higher aggression and boldness) predicted apparent monthly survival probability. Mice that were more aggressive (less docile) had higher survival. Voles that were bolder (less timid) had higher survival, but in the risky forest stands only. Additionally, traits associated with stress coping and de-arousal increased survival probability in both species at high small mammal density but decreased survival at low density. In the two less abundant study species, there was no evidence for an effect of personality traits on survival. Our field experiment provides partial support for our hypothesis: that spatiotemporal fluctuations in refuge abundance and competitor density alter the relationship between personality traits and survival. Our findings also suggest that behaviours associated with stress coping and de-arousal may be subject to density-dependent selection and should be further assessed and incorporated into theory.

The association between personalities, alternative breeding strategies and reproductive success in dunnocks.

Although consistent between-individual differences in behaviour (i.e. animal personality) are ubiquitous in natural populations, relatively few studies have examined how personalities influence the formation of social relationships. Yet, behavioural characteristics of both sexes might be key when it comes to pair-bond formation, and cooperation with partners to successfully rear offspring. We here use a wild population of dunnocks (Prunella modularis) to first investigate whether individuals mate nonrandomly (i.e. assortative mating) with regard to four behavioural traits-flight-initiation distance (FID), provisioning, activity and vigilance-that differ in repeatability and have previously been associated with mating patterns and fitness in other species. Second, we test whether an individual's FID is associated with variability in the dunnocks' mating system (i.e. monogamous pairs vs. polygamous groups). Finally, we determine whether FID and provisioning of males and females associate with their reproductive success. We found no statistical support for assortative mating in FID between males and females. Interestingly, in polygamous groups, co-breeding males differed in their FIDs with dominant alpha males having significantly shorter FIDs compared with subordinate beta-males. Moreover, there was evidence for assortative mating in provisioning for alpha males and females in polygamous groups. We also found that male provisioning influenced reproductive success of both sexes, whereas female provisioning rates only positively correlated with her own but not their partner(s) reproductive output. Our results suggest that personality differences may have important implications for social relationships, the emergence of different mating patterns and ultimately reproductive success within populations.

Predation and parasitism as determinants of animal personalities.

Within the same population, proactive (i.e. bolder, more exploratory, active and aggressive) and reactive (i.e. more timid, less exploratory, less active and more passive) individuals could be hypothetically maintained due a trade-off between foraging and vigilance behaviours, provided that both phenotypes differ in their state (e.g. metabolic rates, body condition or energetic needs). Yet, recent findings indicate that among-individual variation in intrinsic state can explain only a small proportion of variation in behaviour, meaning that other mechanisms, such as the presence of trophically transmitted parasites, might contribute to maintaining inter-individual behavioural differences. Empirical evidence, indeed, suggests strong relationships between certain animal personality traits and parasitic load within host populations. However, the direction of causation between these traits remains unclear: are different behaviours in infected hosts in contrast to uninfected ones the result of manipulation by parasites to increase host predation, or are some personalities inherently more susceptible to infection than others? To better understand the role of parasites in shaping behavioural differences within host populations and examine to what extent parasite manipulation and/or intrinsic differences in parasite susceptibility contribute to maintaining behavioural differences, we used a simulation approach and analysed the change in the frequencies of proactive and reactive individuals over time under different predation and starvation scenarios, when individual phenotype either affected a host's risk of infection or not. We found that in the absence of parasites, predation pressure strongly affected the expression of host personality, but the trade-off between foraging and vigilance behaviours alone could not explain the maintenance of inter-individual behavioural differences without temporal variation in predation pressure. By contrast, in the presence of parasites, the two host phenotypes could coexist within populations even when individuals experienced no temporal variations in predation risk, but only when proactive and reactive hosts were equally susceptible to parasitism. Our findings, thus, indicate that parasites can play an important role in maintaining genetic diversity in their host populations in addition to generating behavioural differences though manipulation.

Psychoactive pollution suppresses individual differences in fish behaviour.

Environmental contamination by pharmaceuticals is global, substantially altering crucial behaviours in animals and impacting on their reproduction and survival. A key question is whether the consequences of these pollutants extend beyond mean behavioural changes, restraining differences in behaviour between individuals. In a controlled, two-year, multigenerational experiment with independent mesocosm populations, we exposed guppies (Poecilia reticulata) to environmentally realistic levels of the ubiquitous pollutant fluoxetine (Prozac). Fish (unexposed: n = 59, low fluoxetine: n = 57, high fluoxetine: n = 58) were repeatedly assayed on four separate occasions for activity and risk-taking behaviour. Fluoxetine homogenized individuals' activity, with individual variation in populations exposed to even low concentrations falling to less than half that in unexposed populations. To understand the proximate mechanism underlying these changes, we tested the relative contribution of variation within and between individuals to the overall decline in individual variation. We found strong evidence that fluoxetine erodes variation in activity between but not within individuals, revealing the hidden consequences of a ubiquitous contaminant on phenotypic variation in fish-likely to impair adaptive potential to environmental change.

The effects of animal personality on the ideal free distribution.

The ideal free distribution (IFD) has been used to predict the distribution of foraging animals in a wide variety of systems. However, its predictions do not always match observed distributions of foraging animals. Instead, we often observe that there are more consumers than predicted in low-quality patches and fewer consumers than predicted in high-quality patches (i.e. undermatching). We examine the possibility that animal personality is one explanation for this undermatching. We first conducted a literature search to determine how commonly studies document the personality distribution of populations. Second, we created a simple individual-based model to conceptually demonstrate why knowing the distribution of personalities is important for studies of populations of foragers in context of the IFD. Third, we present a specific example where we calculate the added time to reach the IFD for a population of mud crabs that has a considerable number of individuals with relatively inactive personalities. We suggest that animal personality, particularly the prevalence of inactive personality types, may inhibit the ability of a population to track changes in habitat quality, therefore leading to undermatching of the IFD. This may weaken the IFD as a predictive model moving forward.

Sociability as a personality trait in animals: methods, causes and consequences.

Within animal populations there is variation among individuals in their tendency to be social, where more sociable individuals associate more with other individuals. Consistent inter-individual variation in 'sociability' is considered one of the major axes of personality variation in animals along with aggressiveness, activity, exploration and boldness. Not only is variation in sociability important in terms of animal personalities, but it holds particular significance for, and can be informed by, two other topics of major interest: social networks and collective behaviour. Further, knowledge of what generates inter-individual variation in social behaviour also holds applied implications, such as understanding disorders of social behaviour in humans. In turn, research using non-human animals in the genetics, neuroscience and physiology of these disorders can inform our understanding of sociability. For the first time, this review brings together insights across these areas of research, across animal taxa from primates to invertebrates, and across studies from both the laboratory and field. We show there are mixed results in whether and how sociability correlates with other major behavioural traits. Whether and in what direction these correlations are observed may differ with individual traits such as sex and body condition, as well as ecological conditions. A large body of evidence provides the proximate mechanisms for why individuals vary in their social tendency. Evidence exists for the importance of genes and their expression, chemical messengers, social interactions and the environment in determining an individual's social tendency, although the specifics vary with species and other variables such as age, and interactions amongst these proximate factors. Less well understood is how evolution can maintain consistent variation in social tendencies within populations. Shifts in the benefits and costs of social tendencies over time, as well as the social niche hypothesis, are currently the best supported theories for how variation in sociability can evolve and be maintained in populations. Increased exposure to infectious diseases is the best documented cost of a greater social tendency, and benefits include greater access to socially transmitted information. We also highlight that direct evidence for more sociable individuals being safer from predators is lacking. Variation in sociability is likely to have broad ecological consequences, but beyond its importance in the spread of infectious diseases, direct evidence is limited to a few examples related to dispersal and invasive species biology. Overall, our knowledge of inter-individual variation in sociability is highly skewed towards the proximate mechanisms. Our review also demonstrates, however, that considering research from social networks and collective behaviour greatly enriches our understanding of sociability, highlighting the need for greater integration of these approaches into future animal personality research to address the imbalance in our understanding of sociability as a personality trait.

Behavioural syndromes and social insects: personality at multiple levels.

Animal personalities or behavioural syndromes are consistent and/or correlated behaviours across two or more situations within a population. Social insect biologists have measured consistent individual variation in behaviour within and across colonies for decades. The goal of this review is to illustrate the ways in which both the study of social insects and of behavioural syndromes has overlapped, and to highlight ways in which both fields can move forward through the synergy of knowledge from each. Here we, (i) review work to date on behavioural syndromes (though not always referred to as such) in social insects, and discuss mechanisms and fitness effects of maintaining individual behavioural variation within and between colonies; (ii) summarise approaches and principles from studies of behavioural syndromes, such as trade-offs, feedback, and statistical methods developed specifically to study behavioural consistencies and correlations, and discuss how they might be applied specifically to the study of social insects; (iii) discuss how the study of social insects can enhance our understanding of behavioural syndromes-research in behavioural syndromes is beginning to explore the role of sociality in maintaining or developing behavioural types, and work on social insects can provide new insights in this area; and (iv) suggest future directions for study, with an emphasis on examining behavioural types at multiple levels of organisation (genes, individuals, colonies, or groups of individuals).