What is the meta-analytic evidence for life-history trade-offs at the genetic level?

Understanding the evolutionary mechanisms underlying the maintenance of individual differences in behavior and physiology is a fundamental goal in ecology and evolution. The pace-of-life syndrome hypothesis is often invoked to explain the maintenance of such within-population variation. This hypothesis predicts that behavioral traits are part of a suite of correlated traits that collectively determine an individual's propensity to prioritize reproduction or survival. A key assumption of this hypothesis is that these traits are underpinned by genetic trade-offs among life-history traits: genetic variants that increase fertility, reproduction and growth might also reduce lifespan. We performed a systematic literature review and meta-analysis to summarize the evidence for the existence of genetic trade-offs between five key life-history traits: survival, growth rate, body size, maturation rate, and fertility. Counter to our predictions, we found an overall positive genetic correlation between survival and other life-history traits and no evidence for any genetic correlations between the non-survival life-history traits. This finding was generally consistent across pairs of life-history traits, sexes, life stages, lab vs. field studies, and narrow- vs. broad-sense correlation estimates. Our study highlights that genetic trade-offs may not be as common, or at least not as easily quantifiable, in animals as often assumed.

Leveraging big data to uncover the eco-evolutionary factors shaping behavioural development.

Mapping the eco-evolutionary factors shaping the development of animals' behavioural phenotypes remains a great challenge. Recent advances in 'big behavioural data' research-the high-resolution tracking of individuals and the harnessing of that data with powerful analytical tools-have vastly improved our ability to measure and model developing behavioural phenotypes. Applied to the study of behavioural ontogeny, the unfolding of whole behavioural repertoires can be mapped in unprecedented detail with relative ease. This overcomes long-standing experimental bottlenecks and heralds a surge of studies that more finely define and explore behavioural-experiential trajectories across development. In this review, we first provide a brief guide to state-of-the-art approaches that allow the collection and analysis of high-resolution behavioural data across development. We then outline how such approaches can be used to address key issues regarding the ecological and evolutionary factors shaping behavioural development: developmental feedbacks between behaviour and underlying states, early life effects and behavioural transitions, and information integration across development.

Predator Group Composition Indirectly Influences Food Web Dynamics through Predator Growth Rates.

AbstractConsiderable theoretical work predicts that intraspecific trait variation can have profound ecological consequences by altering species interactions. Because of their high flexibility, behavioral traits may be especially relevant in mediating how species respond to one another, thus affecting food web dynamics and ecosystem functioning. However, empirical evidence supporting this idea is limited. Here, we generated predator groups where we manipulated the composition of behavioral types within the groups to assess effects on predator growth rates, prey communities, basal resources, and ecosystem functioning in replicated outdoor ponds. Using European perch (Perca fluviatilis), we created three types of predator populations: two where all individuals expressed either bold or shy phenotypes and one that contained a mix of individuals of the two behavioral types. Bold perch grew faster in mixed populations, indicating that predator growth depends on each individual's behavioral type and that of its group members. However, there was no evidence that the behavioral composition of the perch population directly altered the dynamics of lower trophic levels. Instead, final perch biomass, not behavioral composition, had the strongest influence on lower trophic levels. Thus, the central question may not be whether predator behavior matters at all for trophic dynamics but rather when behavioral effects will predominate over effects of other influences, such as predator biomass variation.

Personality-driven life history trade-offs differ in two subpopulations of free-ranging predators.

Consistent individual differences in behaviour (i.e. personality) can be explained in an evolutionary context if they are favoured by life history trade-offs as conceptualized in the pace-of-life syndrome (POLS) hypothesis. Theory predicts that faster-growing individuals suffer higher mortality and that this trade-off is mediated through exploration/risk-taking personality, but empirical support for this remains limited and ambiguous. Equivocal support to the POLS hypothesis suggests that the link between life history and personality may only emerge under certain circumstances. Understanding personality-driven trade-offs would be facilitated by long-term studies in wild populations experiencing different ecological conditions. Here, we tested whether personality measured in semi-captivity was associated with a growth-mortality trade-off via risk-taking in the wild in two subpopulations of juvenile lemon sharks Negaprion brevirostris known to differ in their predator abundance. We expected stronger personality-driven trade-offs in the predator-rich environment as compared to the predator-poor environment. Sharks were captured yearly from 1995 onwards allowing us to obtain long-term data on growth and apparent survival in each subpopulation. We then used a novel open-field assay to test sharks for exploration personality yearly from 2012 to 2017. A subset of the tested sharks was monitored in the field using telemetry to document risk-taking behaviours. We tested (a) if fast explorers in captivity took more risks and grew faster in the wild and (b) if natural selection acted against more explorative, faster-growing sharks. In the subpopulation with fewer predators, more explorative sharks in captivity took more risks in the wild and grew faster. In turn, larger, fast-growing sharks had lower apparent survival. In the predator-rich subpopulation, despite finding selection on fast growth, we found no link between exploration personality and the growth-mortality trade-off. Our study demonstrates that the association between personality and life history is favoured in some ecological contexts but not in others. We identify predator and resource abundance as two main potential drivers of the personality-mediated trade-off and emphasize that future work on the POLS hypothesis would benefit from an approach integrating behaviour and life history across ecological conditions.

Individual differences in behaviour explain variation in survival: a meta-analysis.

Research focusing on among-individual differences in behaviour ('animal personality') has been blooming for over a decade. Central theories explaining the maintenance of such behavioural variation posits that individuals expressing greater "risky" behaviours should suffer higher mortality. Here, for the first time, we synthesize the existing empirical evidence for this key prediction. Our results did not support this prediction as there was no directional relationship between riskier behaviour and greater mortality; however there was a significant absolute relationship between behaviour and survival. In total, behaviour explained a significant, but small, portion (5.8%) of the variance in survival. We also found that risky (vs. "shy") behavioural types live significantly longer in the wild, but not in the laboratory. This suggests that individuals expressing risky behaviours might be of overall higher quality but the lack of predation pressure and resource restrictions mask this effect in laboratory environments. Our work demonstrates that individual differences in behaviour explain important differences in survival but not in the direction predicted by theory. Importantly, this suggests that models predicting behaviour to be a mediator of reproduction-survival trade-offs may need revision and/or empiricists may need to reconsider their proxies of risky behaviours when testing such theory.

Repeatable group differences in the collective behaviour of stickleback shoals across ecological contexts.

Establishing how collective behaviour emerges is central to our understanding of animal societies. Previous research has highlighted how universal interaction rules shape collective behaviour, and that individual differences can drive group functioning. Groups themselves may also differ considerably in their collective behaviour, but little is known about the consistency of such group variation, especially across different ecological contexts that may alter individuals' behavioural responses. Here, we test if randomly composed groups of sticklebacks differ consistently from one another in both their structure and movement dynamics across an open environment, an environment with food, and an environment with food and shelter. Based on high-resolution tracking data of the free-swimming shoals, we found large context-associated changes in the average behaviour of the groups. But despite these changes and limited social familiarity among group members, substantial and predictable behavioural differences between the groups persisted both within and across the different contexts (group-level repeatability): some groups moved consistently faster, more cohesively, showed stronger alignment and/or clearer leadership than other groups. These results suggest that among-group heterogeneity could be a widespread feature in animal societies. Future work that considers group-level variation in collective behaviour may help understand the selective pressures that shape how animal collectives form and function.

Individual and Group Performance Suffers from Social Niche Disruption.

The social niche specialization hypothesis predicts that animal personalities emerge as a result of individuals occupying different social niches within a group. Here we track individual personality and performance and collective performance among groups of social spiders where we manipulated the familiarity of the group members. We show that individual personalities, as measured by consistent individual differences in boldness behavior, strengthen with increasing familiarity and that these personalities can be disrupted by a change in group membership. Changing group membership negatively impacted both individual and group performance. Individuals in less familiar groups lost weight, and these groups were less successful at performing vital collective tasks. These results provide a mechanism for the evolution of stable social groups by demonstrating that social niche reestablishment carries a steep cost for both individuals and groups. Social niche specialization may therefore provide a potential first step on the path toward more organized social systems.

The making of winners (and losers): how early dominance interactions determine adult social structure in a clonal fish.

Across a wide range of animal taxa, winners of previous fights are more likely to keep winning future contests, just as losers are more likely to keep losing. At present, such winner and loser effects are considered to be fairly transient. However, repeated experiences with winning and/or losing might increase the persistence of these effects, generating long-lasting consequences for social structure. To test this, we exposed genetically identical individuals of a clonal fish, the Amazon molly (Poecilia formosa), to repeated winning and/or losing dominance interactions during the first two months of their life. We subsequently investigated whether these experiences affected the fish's ability to achieve dominance in a hierarchy five months later after sexual maturity, a major life-history transition. Individuals that had only winning interactions early in life consistently ranked at the top of the hierarchy. Interestingly, individuals with only losing experience tended to achieve the middle dominance rank, whereas individuals with both winning and losing experiences generally ended up at the bottom of the hierarchy. In addition to demonstrating that early social interactions can have dramatic and long-lasting consequences for adult social behaviour and social structure, our work also shows that higher cumulative winning experience early in life can counterintuitively give rise to lower social rank later in life.

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider.

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.

Persistent social interactions beget more pronounced personalities in a desert-dwelling social spider.

The social niche specialization hypothesis predicts that repeated social interactions will generate social niches within groups, thereby promoting consistent individual differences in behaviour. Current support for this hypothesis is mixed, probably because the importance of social niches is dependent upon the ecology of the species. We test whether repeated interactions among group mates generate consistent individual differences in boldness in the social spider, Stegodyphus dumicola. In support of the social niche specialization hypothesis, we found that consistent individual differences in boldness increased with longer group tenure. Interestingly, these differences took longer to appear than in previous work suggesting this species needs more persistent social interactions to shape its behaviour. Recently disturbed colonies were shyer than older colonies, possibly reflecting differences in predation risk. Our study emphasizes the importance of the social environment in generating animal personalities, but also suggests that the pattern of personality development can depend on subtle differences in species' ecologies.

Behavioral responses of a clonal fish to perceived predation risk.

Predation threat is a major driver of behavior in many prey species. Animals can recognize their relative risk of predation based on cues in the environment, including visual and/or chemical cues released by a predator or from its prey. When threat of predation is high, prey often respond by altering their behavior to reduce their probability of detection and/or capture. Here, we test how a clonal fish, the Amazon molly (Poecilia formosa), behaviorally responds to predation cues. We measured aggressive and social behaviors both under 'risk', where chemical cues from predatory fish and injured conspecifics were present, and control contexts (no risk cues present). We predicted that mollies would exhibit reduced aggression towards a simulated intruder and increased sociability under risk contexts as aggression might increase their visibility to a predator and shoaling should decrease their chance of capture through the dilution effect. As predicted, we found that Amazon mollies spent more time with a conspecific when risk cues were present, however they did not reduce their aggression. This highlights the general result of the 'safety in numbers' behavioral response that many small shoaling species exhibit, including these clonal fish, which suggests that mollies may view this response as a more effective anti-predator response compared to limiting their detectability by reducing aggressive conspecific interactions.

Competition avoidance drives individual differences in response to a changing food resource in sticklebacks.

Within the same population, individuals often differ in how they respond to changes in their environment. A recent series of models predicts that competition in a heterogeneous environment might promote between-individual variation in behavioural plasticity. We tested groups of sticklebacks in patchy foraging environments that differed in the level of competition. We also tested the same individuals across two different social groups and while alone to determine the social environment's influence on behavioural plasticity. In support of model predictions, individuals consistently differed in behavioural plasticity when the presence of conspecifics influenced the potential payoffs of a foraging opportunity. Whether individuals maintained their level of behavioural plasticity when placed in a new social group depended on the environmental heterogeneity. By explicitly testing predictions of recent theoretical models, we provide evidence for the types of ecological conditions under which we would expect, and not expect, variation in behavioural plasticity to be favoured.

A multi-scale review of the dynamics of collective behaviour: from rapid responses to ontogeny and evolution.

Collective behaviours, such as flocking in birds or decision making by bee colonies, are some of the most intriguing behavioural phenomena in the animal kingdom. The study of collective behaviour focuses on the interactions between individuals within groups, which typically occur over close ranges and short timescales, and how these interactions drive larger scale properties such as group size, information transfer within groups and group-level decision making. To date, however, most studies have focused on snapshots, typically studying collective behaviour over short timescales up to minutes or hours. However, being a biological trait, much longer timescales are important in animal collective behaviour, particularly how individuals change over their lifetime (the domain of developmental biology) and how individuals change from one generation to the next (the domain of evolutionary biology). Here, we give an overview of collective behaviour across timescales from the short to the long, illustrating how a full understanding of this behaviour in animals requires much more research attention on its developmental and evolutionary biology. Our review forms the prologue of this special issue, which addresses and pushes forward understanding the development and evolution of collective behaviour, encouraging a new direction for collective behaviour research. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Conformity and differentiation are two sides of the same coin.

Variation between individuals is a key component of selection and hence evolutionary change. Social interactions are important drivers of variation, potentially making behaviour more similar (i.e., conform) or divergent (i.e., differentiate) between individuals. While documented across a wide range of animals, behaviours and contexts, conformity and differentiation are typically considered separately. Here, we argue that rather than independent concepts, they can be integrated onto a single scale that considers how social interactions drive changes in interindividual variance within groups: conformity reduces variance within groups while differentiation increases it. We discuss the advantages of placing conformity and differentiation at different ends of a single scale, allowing for a deeper understanding of the relationship between social interactions and interindividual variation.

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.

The emergence and development of behavioral individuality in clonal fish.

Behavioral individuality is a ubiquitous phenomenon in animal populations, yet the origins and developmental trajectories of individuality, especially very early in life, are still a black box. Using a high-resolution tracking system, we mapped the behavioral trajectories of genetically identical fish (Poecilia formosa), separated immediately after birth into identical environments, over the first 10 weeks of their life at 3 s resolution. We find that (i) strong behavioral individuality is present at the very first day after birth, (ii) behavioral differences at day 1 of life predict behavior up to at least 10 weeks later, and (iii) patterns of individuality strengthen gradually over developmental time. Our results establish a null model for how behavioral individuality can develop in the absence of genetic and environmental variation and provide experimental evidence that later-in-life individuality can be strongly shaped by factors pre-dating birth like maternal provisioning, epigenetics and pre-birth developmental stochasticity.

Integrating Behavior in Life-History Theory: Allocation versus Acquisition?

Central theories explaining the maintenance of individual differences in behavior build on the assumption that behavior mediates life-history trade-offs between current and future reproduction. However, current empirical evidence does not robustly support this assumption. This mismatch might be because current theory is not clear about the role of behavior in individual allocation versus acquisition of resources, hindering empirical testing. The relative importance of allocation compared to acquisition is a key feature of classic life-history theory, but appears to have been lost in translation in recent developments of life-history theory involving behavior. We argue that determining the relative balance between variation in resource allocation and acquisition, and the role of behavior in this process, will help to build more robust and precise predictions.