Predation risk shapes among- and within-individual variation in behavior in poison frog tadpoles

Within populations, individuals often show repeatable variation in behaviour, called 'animal personality'. In the last few decades, numerous empirical studies have attempted to elucidate the mechanisms maintaining this variation, such as life-history trade-offs. Theory predicts that among-individual variation in behavioural traits could be maintained if traits that are positively associated with reproduction are simultaneously associated with decreased survival, such that different levels of behavioural expression lead to the same net fitness outcome. However, variation in resource acquisition may also be important in mediating the relationship between individual behaviour and fitness components (survival and reproduction). For example, if certain phenotypes (e.g. dominance or aggressiveness) are associated with higher resource acquisition, those individuals may have both higher reproduction and higher survival, relative to others in the population. When individuals differ in their ability to acquire resources, trade-offs are only expected to be observed at the within-individual level (i.e. for a given amount of resource, if an individual increases its allocation to reproduction, it comes at the cost of allocation to survival, and vice versa), while among individuals traits that are associated with increased survival may also be associated with increased reproduction. We performed a systematic review and meta-analysis, asking: (i) do among-individual differences in behaviour reflect among-individual differences in resource acquisition and/or allocation, and (ii) is the relationship between behaviour and fitness affected by the type of behaviour and the testing environment? Our meta-analysis consisted of 759 estimates from 193 studies. Our meta-analysis revealed a positive correlation between pairs of estimates using both survival and reproduction as fitness proxies. That is, for a given study, behaviours that were associated with increased reproduction were also associated with increased survival, suggesting that variation in behaviour at the among-individual level largely reflects differences among individuals in resource acquisition. Furthermore, we found the same positive correlation between pairs of estimates using both survival and reproduction as fitness proxies at the phenotypic level. This is significant because we also demonstrated that these phenotypic correlations primarily reflect within-individual correlations. Thus, even when accounting for among-individual differences in resource acquisition, we did not find evidence of trade-offs at the within-individual level. Overall, the relationship between behaviour and fitness proxies was not statistically different from zero at the among-individual, phenotypic, and within-individual levels; this relationship was not affected by behavioural category nor by the testing condition. Our meta-analysis highlights that variation in resource acquisition may be more important in driving the relationship between behaviour and fitness than previously thought, including at the within-individual level. We suggest that this may come about via heterogeneity in resource availability or age-related effects, with higher resource availability and/or age leading to state-dependent shifts in behaviour that simultaneously increase both survival and reproduction. We emphasize that future studies examining the mechanisms maintaining behavioural variation in populations should test the link between behavioural expression and resource acquisition - both within and among individuals. Such work will allow the field of animal personality to develop specific predictions regarding the mediating effect of resource acquisition on the fitness consequences of individual behaviour.

The relationship between risk-prone behavior and growth is central to tradeoff models that explain the existence and maintenance of among-individual variation in behavior (i.e. animal personality). These models posit positive relationships between among-individual variation in risk-prone behaviors and growth, yet how the strength and direction of such relationships depend on ecological conditions is unclear. We tested how different levels of predation risk from crayfish (Faxonius limosus) mediate the association between among-individual variation in snail (Helisoma trivolvis) boldness (emergence time) and growth in shell size. We found that crayfish predation risk reduced snail growth but that the effect of snail boldness on individual growth was context-dependent—snail boldness was unrelated to growth in the absence of risk and under high risk, but shy snails grew faster than bold snails under low predation risk. Other traits (snail size, body condition, and intrinsic growth rate measured under ad libitum food conditions) failed to explain snail growth variation under any risk level. Though opposite to the prediction of tradeoff models, enhanced growth of shy snails could function as a predator defense mechanism that protects their prospects for future reproduction consistent with the underlying premise of tradeoff models. Thus, our results highlight the importance of accounting for ecological conditions in understanding behavior–life history associations.

Criteria for acceptable studies of animal personality and behavioural syndromes

The study of consistent between-individual behavioural variation in single (animal personality) and across two or more behavioural traits (behavioural syndrome) is a central topic of behavioural ecology. Besides behavioural type (individual mean behaviour), behavioural predictability (environment-independent within-individual behavioural variation) is now also seen as an important component of individual behavioural strategy. Research focus is still on the ‘Big Five’ traits (activity, exploration, risk-taking, sociability and aggression), but another prime candidate to integrate to the personality framework is behavioural thermoregulation in small-bodied poikilotherms. Here, we found animal personality in thermoregulatory strategy (selected body temperature, voluntary thermal maximum, setpoint range) and ‘classic’ behavioural traits (activity, sheltering, risk-taking) in common lizards (Zootoca vivipara). Individual state did not explain the between-individual variation. There was a positive behavioural type—behavioural predictability correlation in selected body temperature. Besides an activity—risk-taking syndrome, we also found a risk-taking—selected body temperature syndrome. Our results suggest that animal personality and behavioural syndrome are present in common lizards, both including thermoregulatory and ‘classic’ behavioural traits, and selecting high body temperature with high predictability is part of the risk-prone behavioural strategy. We propose that thermoregulatory behaviour should be considered with equal weight to the ‘classic’ traits in animal personality studies of poikilotherms employing active behavioural thermoregulation.

We review the evidence for a link between consistent among-individual variation in behaviour (animal personality) and the ability to win contests over limited resources. Explorative and bold behaviours often covary with contest behaviour and outcome, although there is evidence that the structure of these 'behavioural syndromes' can change across situations. Aggression itself is typically repeatable, but also subject to high within-individual variation as a consequence of plastic responses to previous fight outcomes and opponent traits. Common proximate mechanisms (gene expression, endocrine control and metabolic rates) may underpin variation in both contest behaviour and general personality traits. Given the theoretical links between the evolution of fighting and of personality, we suggest that longitudinal studies of contest behaviour, combining behavioural and physiological data, would be a useful context for the study of animal personalities.

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.

Life history theory predicts that individuals will differ in their risk-taking behavior according to their expected future fitness. Understanding consequences of such individual variation within a behavioral trait is crucial in explaining potential trade-offs between different traits and in predicting future dynamics in changing environments. Here, we studied individuals in a wild arctic fox population to explore if (1) individual variation in risk-taking behaviors of adult arctic foxes and in stress-dealing behaviors of their juveniles exist and are consistent over time to verify the existence of personality traits; (2) those behavioral traits in adults and juveniles are correlated; (3) they can explain fitness-related components (i.e., juvenile physical condition, mortality rate). We presented simple field experiments assessing behavioral traits by observing adult reactions toward approaching observers, and juvenile behaviors while trapping. Through the experiments, we found highly consistent individual variation of adults in vigilance and boldness levels, and more flexible juvenile behavioral traits categorized as investigating, passive, and escaping. The offspring of bolder adults exhibited more investigating behaviors and were less passive than the offspring of shy adults. Juvenile physical condition was not related to their mortality nor any behavioral traits of either parents or themselves. Lastly, highly investigating and active juveniles with bold parents had significantly lower mortality rates. This shows that interactions between parent personality and juvenile behavioral traits affect a fitness-related component in the life history of individuals.Significance statementThe recent surge of interest in consistent individual difference in behavior, also called as animal personality, has already focused on its fitness consequences, but few studies have investigated the interactions between parent and offspring personality, and their ecological consequences. Moreover, this has rarely been studied in wild canids. The arctic fox is a charismatic species showing wide individual variation in behaviors. They live in highly fluctuating tundra ecosystems providing different selection regimes, making it even more eco-evolutionarily intriguing. Yet, few studies looked into behavioral traits and their importance in this system. While introducing simple methods to improve personality research in the wild, we provide a unique example of how variation in both parents and their juveniles collectively works for group dynamics in a cyclic population. This provides a firm basic for understanding behavior-mediated dynamics and opens up broader questions on how fluctuating environments exert varying pressures on individual differences.

Individuals frequently differ consistently from one another in their average behaviours (i.e. 'animal personality') and in correlated suites of consistent behavioural responses (i.e. 'behavioural syndromes'). However, understanding the evolutionary basis of this (co)variation has lagged behind demonstrations of its presence. This lag partially stems from comparative methods rarely being used in the field. Consequently, much of the research on animal personality has relied on 'adaptive stories' focused on single species and populations. Here, we used a comparative approach to examine the role of phylogeny in shaping patterns of average behaviours, behavioural variation and behavioural correlations. In comparing the behaviours and behavioural variation for five species of Gryllid crickets, we found that phylogeny shaped average behaviours and behavioural (co)variation. Despite differences among species, behavioural responses and variation were most similar among more closely related species. These results suggest that phylogenetic constraints play an important role in the expression of animal personalities and behavioural syndromes and emphasize the importance of examining evolutionary explanations within a comparative framework.

The repeatable among-individual variation in behavior (animal personality) is considered to affect fitness. The variation in personality traits is shaped by complex evolutionary mechanisms involving energy allocation and resource acquisition. However, an association between personality and individual performance in energy gain in the natural environment still seems underexplored. The aim of our study was to test a hypothesis that consistent individual variation in behavior affects the energy acquisition of unpredictable food resources. We predicted that more explorative individuals would be finding ephemeral food resources with higher probability than those less explorative. The quasi-experiment with ‘random-walking-feeders’ was performed to assess the use of unpredictable food resources in the natural habitat occupied by free-ranging arboreal rodents — edible dormice Glis glis. A repeated open field test at laboratory conditions was conducted to assess whether male dormice show consistent among-individual variation in behavior. The open field test analysis indicated two main components of dormice behavior: exploration and boldness, from which only the first one was repeatable and thus considered as a component of animal personality. The probability of finding a feeder increased with exploration, independently of dormice age and body size. The results indicate that exploration can be considered an adaptive trait that improves energy acquisition. We suggest that the behavioral among-individual variation within populations persists due to the usage of distinct foraging strategies in the face of fluctuations in food resources availability.

Animal personality variation is characterized by among-individual differences in behavior that are consistent across ecological contexts and over time. However, processes influencing the amount of personality variation are not well understood. In this study, we tested 1 hypothesized mechanism through which variation in personalities may be maintained: spatial variation in natural selection. Through laboratory behavioral assays, we demonstrated that 2 personality traits—exploration and risk taking—are moderately repeatable for wavy turban snails, Megastraea undosa (mean repeatability values = 0.320 and 0.297, respectively). We also found that there could be up to a 1.7-fold difference in among-individual variation in behavior for different populations. We next measured natural selection on these behavioral traits by experimentally transporting assayed snails to field populations in a mark-recapture study to examine the relationships between behavioral traits and growth and survival. We studied 4 populations: 2 that had an abundance of slow-moving predators (whelks, sea stars) and 2 where slow-moving predators were absent and the major predators were fast-moving species (lobsters). Selection on behavioral traits varied significantly among local populations. Depending on location, patterns of selection could be predominantly stabilizing, disruptive, or correlational. Fitness surfaces were not necessarily similar for local populations with similar predator communities, and nearby locations could have strikingly different patterns of selection. Behavioral tendencies that were associated with high fitness in 1 population could be neutral or associated with low fitness in a nearby population. Such effects likely contribute to maintaining variation in animal personality within the broader population.

Animal personality

Growing interest in proximate and ultimate causes and consequences of between- and within-individual variation in labile components of the phenotype - such as behaviour or physiology - characterizes current research in evolutionary ecology. The study of individual variation requires tools for quantification and decomposition of phenotypic variation into between- and within-individual components. This is essential as variance components differ in their ecological and evolutionary implications. We provide an overview of how mixed-effect models can be used to partition variation in, and correlations among, phenotypic attributes into between- and within-individual variance components. Optimal sampling schemes to accurately estimate (with sufficient power) a wide range of repeatabilities and key (co)variance components, such as between- and within-individual correlations, are detailed. Mixed-effect models enable the usage of unambiguous terminology for patterns of biological variation that currently lack a formal statistical definition (e.g. 'animal personality' or 'behavioural syndromes'), and facilitate cross-fertilisation between disciplines such as behavioural ecology, ecological physiology and quantitative genetics.

In our rapidly changing world, understanding how species respond to shifting conditions is of paramount importance. Pharmaceutical pollutants are widespread in aquatic ecosystems globally, yet their impacts on animal behaviour, life-history and reproductive allocation remain poorly understood, especially in the context of intraspecific variation in ecologically important traits that facilitate species' adaptive capacities. We test whether a widespread pharmaceutical pollutant, fluoxetine (Prozac), disrupts the trade-off between individual-level (co)variation in behavioural, life-history and reproductive traits of freshwater fish. We exposed the progeny of wild-caught guppies (Poecilia reticulata) to three field-relevant levels of fluoxetine (mean measured concentrations: 0, 31.5 and 316 ng/L) for 5 years, across multiple generations. We used 12 independent laboratory populations and repeatedly quantified activity and risk-taking behaviour of male guppies, capturing both mean behaviours and variation within and between individuals across exposure treatments. We also measured key life-history traits (body condition, coloration and gonopodium size) and assessed post-copulatory sperm traits (sperm vitality, number and velocity) that are known to be under strong sexual selection in polyandrous species. Intraspecific (co)variation of these traits was analysed using a comprehensive, multivariate statistical approach. Fluoxetine had a dose-specific (mean) effect on the life-history and sperm trait of guppies: low pollutant exposure altered male body condition and increased gonopodium size, but reduced sperm velocity. At the individual level, fluoxetine reduced the behavioural plasticity of guppies by eroding their within-individual variation in both activity and risk-taking behaviour. Fluoxetine also altered between-individual correlations in pace-of-life syndrome traits: it triggered the emergence of correlations between behavioural and life-history traits (e.g. activity and body condition) and between life-history and sperm traits (e.g. gonopodium size and sperm vitality), but collapsed other between-individual correlations (e.g. activity and gonopodium size). Our results reveal that chronic exposure to global pollutants can affect phenotypic traits at both population and individual levels, and even alter individual-level correlations among such traits in a dose-specific manner. We discuss the need to integrate individual-level analyses and test behaviour in association with life-history and reproductive traits to fully understand how animals respond to human-induced environmental change.

Temporal consistency and behavioural variation: a long-term study of exploration and activity in Microcebus murinus

Animal personality, characterized by consistent individual variation in behavioral expression, and behavioral syndromes, underlying correlations between behaviors, have been studied in numerous vertebrate and invertebrate species, including ants. Yet, research on the evolutionary origins of this (co)variation has progressed more slowly than studies showing its occurrence, partly due to varying methodologies preventing comparisons among species. In this study, we applied a comparative framework to investigate patterns of average behaviors and behavioral variation in four ant species belonging to two different subfamilies: Formica fusca and Camponotus aethiops (Formicinae), Aphaenogaster senilis and Messor barbarus (Myrmicinae). We analyzed four behaviors reflecting the responses of ants in foraging or social contexts: exploratory activity, reaction-to-prey, reaction-to-brood, and sociability. All traits except sociability showed moderate to high repeatability in each species. When comparing species for each personality trait, in terms of both average behavioral expression and among-individual variance, we found evidence that phylogeny possibly influences these parameters in the reaction-to-prey test, with closely related species showing more similar behavioral profiles. Other differences among species appear to stem from ecological differences. Evidence of behavioral syndromes was found only in A. senilis, with clear correlation between reaction-to-brood and reaction-to-prey, as well as between reaction-to-brood and exploratory activity. Taken together, our findings suggest that our protocol is robust for assessing personality traits across different ant species and that phylogeny may influence the expression of inter-individual differences in certain behavioral traits. These results call for further studies exploring the evolutionary basis of animal personality within a comparative framework.