Social interactions generate complex selection patterns in virtual worlds.

Understanding the influence of social interactions on individual fitness is key to improving our predictions of phenotypic evolution. However, we often overlook the different components of selection regimes arising from interactions among organisms, including social, correlational, and indirect selection. This is due to the challenging sampling efforts required in natural populations to measure phenotypes expressed during interactions and individual fitness. Furthermore, behaviours are crucial in mediating social interactions, yet few studies have explicitly quantified these selection components on behavioural traits. In this study, we capitalize on an online multiplayer videogame as a source of extensive data recording direct social interactions among prey, where prey collaborate to escape a predator in realistic ecological settings. We estimate natural and social selection and their contribution to total selection on behavioural traits mediating competition, cooperation, and predator-prey interactions. Behaviours of other prey in a group impact an individual's survival, and thus are under social selection. Depending on whether selection pressures on behaviours are synergistic or conflicting, social interactions enhance or mitigate the strength of natural selection, although natural selection remains the main driving force. Indirect selection through correlations among traits also contributed to the total selection. Thus, failing to account for the effects of social interactions and indirect selection would lead to a misestimation of the total selection acting on traits. Dissecting the contribution of each component to the total selection differential allowed us to investigate the causal mechanisms relating behaviour to fitness and quantify the importance of the behaviours of conspecifics as agents of selection. Our study emphasizes that social interactions generate complex selective regimes even in a relatively simple ecological environment.

The evolution of prey-attraction strategies in spiders: the interplay between foraging and predator avoidance.

Lures and other adaptations for prey attraction are particularly interesting from an evolutionary viewpoint because they are characterized by correlational selection, involve multicomponent signals, and likely reflect a compromise between maximizing conspicuousness to prey while avoiding drawing attention of enemies and predators. Therefore, investigating the evolution of lure and prey-attraction adaptations can help us understand a larger set of traits governing interactions among organisms. We review the literature focusing on spiders (Araneae), which is the most diverse animal group using prey attraction and show that the evolution of prey-attraction strategies must be driven by a trade-off between foraging and predator avoidance. This is because increasing detectability by potential prey often also results in increased detectability by predators higher in the food chain. Thus increasing prey attraction must come at a cost of increased risk of predation. Given this trade-off, we should expect lures and other prey-attraction traits to remain suboptimal despite a potential to reach an optimal level of attractiveness. We argue that the presence of this trade-off and the multivariate nature of prey-attraction traits are two important mechanisms that might maintain the diversity of prey-attraction strategies within and between species. Overall, we aim to stimulate research on this topic and progress in our general understanding of the diversity of predator and prey interactions.

Injected serotonin decreases foraging aggression in black widow spiders (Latrodectus hesperus), but dopamine has no effect.

A fundamental goal of animal behavior research is to discover the proximate mechanisms driving individual behavioral differences. Biogenic amines are known to mediate various aspects of behavior across many species, including aggression, one of the most commonly measured behavioral traits in animals. Arthropods provide an excellent system to manipulate biogenic amines and quantify subsequent behavioral changes. Here, we investigated the role of dopamine (DA) and serotonin (5-HT) on foraging aggression in western black widow spiders (Latrodectus hesperus), as measured by the number of attacks on a simulated prey animal in the web. We injected spiders with DA or 5-HT and then quantified subsequent changes in behavior over 48 h. Based on previous work on insects and spiders, we hypothesized that increasing DA levels would increase aggression, while increasing 5-HT would decrease aggression. We found that injection of 5-HT did decrease black widow foraging aggression, but DA had no effect. This could indicate that the relationship between DA and aggression is complex, or that DA may not play as important a role in driving aggressive behavior as previously thought, at least in black widow spiders. Aggressive behavior is likely also influenced by other factors, such as inter-individual differences in genetics, metabolic rates, environment, and other neurohormonal controls.

Anticipated effects of abiotic environmental change on intraspecific social interactions.

Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.

The role of habitat configuration in shaping animal population processes: a framework to generate quantitative predictions.

By shaping where individuals move, habitat configuration can fundamentally structure animal populations. Yet, we currently lack a framework for generating quantitative predictions about the role of habitat configuration in modulating population outcomes. To address this gap, we propose a modelling framework inspired by studies using networks to characterize habitat connectivity. We first define animal habitat networks, explain how they can integrate information about the different configurational features of animal habitats, and highlight the need for a bottom-up generative model that can depict realistic variations in habitat potential connectivity. Second, we describe a model for simulating animal habitat networks (available in the R package AnimalHabitatNetwork), and demonstrate its ability to generate alternative habitat configurations based on empirical data, which forms the basis for exploring the consequences of alternative habitat structures. Finally, we lay out three key research questions and demonstrate how our framework can address them. By simulating the spread of a pathogen within a population, we show how transmission properties can be impacted by both local potential connectivity and landscape-level characteristics of habitats. Our study highlights the importance of considering the underlying habitat configuration in studies linking social structure with population-level outcomes.

Social selection acts on behavior and body mass but does not contribute to the total selection differential in eastern chipmunks.

Through social interactions, phenotypes of conspecifics can affect an individual's fitness, resulting in social selection. Social selection is assumed to represent a strong and dynamic evolutionary force that can act with or in opposition to natural selection. Few studies, however, have estimated social selection and its contribution to total selection in the wild. We estimated natural and social selection gradients on exploration, docility, and body mass, and their contribution to selection differentials, in a wild eastern chipmunk population (Tamias striatus). We applied trait-based multiple regression models derived from classical phenotypic selection analyses, which allowed us to include several social partners (i.e., neighbors). We detected social selection gradients on female docility and male body mass, indicating that female with docile neighbors and males with large neighbors had lower fitness. In both sexes, social selection gradients varied with the season. However, we found no phenotypic assortment or disassortment for the studied traits. Social selection gradients, therefore, did not contribute to total selection differentials, and natural selection alone could drive phenotypic changes. Evaluating the factors that drive the evolution of the covariance between interacting phenotypes is necessary to understand the role of social selection as an evolutionary force.

Warming-induced shifts in amphibian phenology and behavior lead to altered predator-prey dynamics.

Climate change-induced phenological variation in amphibians can disrupt time-sensitive processes such as breeding, hatching, and metamorphosis, and can consequently alter size-dependent interactions such as predation. Temperature can further alter size-dependent, predator-prey relationships through changes in species' behavior. We thus hypothesized that phenological shifts due to climate warming would alter the predator-prey dynamic in a larval amphibian community through changes in body size and behavior of both the predator and prey. We utilized an amphibian predator-prey system common to the montane wetlands of the U.S. Pacific Northwest: the long-toed salamander (Ambystoma macrodactylum) and its anuran prey, the Pacific chorus frog (Pseudacris regilla). We conducted predation trials to test if changes in predator phenology and environmental temperature influence predation success. We simulated predator phenological shifts using different size classes of the long-toed salamander representing an earlier onset of breeding while using spring temperatures corresponding to early and mid-season larval rearing conditions. Our results indicated that the predator-prey dynamic was highly dependent upon predator phenology and temperature, and both acted synergistically. Increased size asymmetry resulted in higher tadpole predation rates and tadpole tail damage. Both predators and prey altered activity and locomotor performance in warmer treatments. Consequently, behavioral modifications resulted in decreased survival rates of tadpoles in the presence of large salamander larvae. If predators shift to breed disproportionately earlier than prey due to climate warming, this has the potential to negatively impact tadpole populations in high-elevation amphibian assemblages through changes in predation rates mediated by behavior.

Linking the fine-scale social environment to mating decisions: a future direction for the study of extra-pair paternity.

Variation in extra-pair paternity (EPP) among individuals of the same population could result from stochastic demography or from individual differences in mating strategies. Although the adaptive value of EPP has been widely studied, much less is known about the characteristics of the social environment that drive the observed patterns of EPP. Here, we demonstrate how concepts and well-developed tools for the study of social behaviour (such as social network analysis) can enhance the study of extra-pair mating decisions (focussing in particular on avian mating systems). We present several hypotheses that describe how characteristics of the social environment in which individuals are embedded might influence the levels of EPP in a socially monogamous population. We use a multi-level social approach (Hinde, 1976) to achieve a detailed description of the social structure and social dynamics of individuals in a group. We propose that the pair-bond, the direct (local) social environment and the indirect (extended) social environment, can contribute in different ways to the variation observed in the patterns of EPP, at both the individual and the population level. A strength of this approach is that it integrates into the analysis (indirect) interactions with all potential mates in a population, thus extending the current framework to study extra-pair mating behaviour. We also encourage the application of social network methods such as temporal dynamic analysis to depict temporal changes in the patterns of interactions among individuals in a group, and to study how this affects mating behaviour. We argue that this new framework will contribute to a better understanding of the proximate mechanisms that drive variation in EPP within populations in socially monogamous species, and might ultimately provide insights into the evolution and maintenance of mating systems.

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes.

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.

Correlational selection on personality and social plasticity: morphology and social context determine behavioural effects on mating success.

Despite a central line of research aimed at quantifying relationships between mating success and sexually dimorphic traits (e.g., ornaments), individual variation in sexually selected traits often explains only a modest portion of the variation in mating success. Another line of research suggests that a significant portion of the variation in mating success observed in animal populations could be explained by correlational selection, where the fitness advantage of a given trait depends on other components of an individual's phenotype and/or its environment. We tested the hypothesis that interactions between multiple traits within an individual (phenotype dependence) or between an individual's phenotype and its social environment (context dependence) can select for individual differences in behaviour (i.e., personality) and social plasticity. To quantify the importance of phenotype- and context-dependent selection on mating success, we repeatedly measured the behaviour, social environment and mating success of about 300 male stream water striders, Aquarius remigis. Rather than explaining individual differences in long-term mating success, we instead quantified how the combination of a male's phenotype interacted with the immediate social context to explain variation in hour-by-hour mating decisions. We suggest that this analysis captures more of the mechanisms leading to differences in mating success. Males differed consistently in activity, aggressiveness and social plasticity. The mating advantage of these behavioural traits depended on male morphology and varied with the number of rival males in the pool, suggesting mechanisms selecting for consistent differences in behaviour and social plasticity. Accounting for phenotype and context dependence improved the amount of variation in male mating success we explained statistically by 30-274%. Our analysis of the determinants of male mating success provides important insights into the evolutionary forces that shape phenotypic variation. In particular, our results suggest that sexual selection is likely to favour individual differences in behaviour, social plasticity (i.e., individuals adjusting their behaviour), niche preference (i.e., individuals dispersing to particular social conditions) or social niche construction (i.e., individuals modifying the social environment). The true effect of sexual traits can only be understood in interaction with the individual's phenotype and environment.

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 contribution of developmental experience vs. condition to life history, trait variation and individual differences.

1. Developmental experience, for example food abundance during juvenile stages, is known to affect life history and behaviour. However, the life history and behavioural consequences of developmental experience have rarely been studied in concert. As a result, it is still unclear whether developmental experience affects behaviour through changes in life history, or independently of it. 2. The effect of developmental experience on life history and behaviour may also be masked or affected by individual condition during adulthood. Thus, it is critical to tease apart the effects of developmental experience and current individual condition on life history and behaviour. 3. In this study, we manipulated food abundance during development in the western black widow spider, Latrodectus hesperus, by rearing spiders on either a restricted or ad lib diet. We separated developmental from condition-dependent effects by assaying adult foraging behaviour (tendency to attack prey and to stay on out of the refuge following an attack) and web structure multiple times under different levels of satiation following different developmental treatments. 4. Spiders reared under food restriction matured slower and at a smaller size than spiders reared in ad lib conditions. Spiders reared on a restricted diet were more aggressive towards prey and built webs structured for prey capture, while spiders reared on an ad lib diet were less aggressive and built safer webs. Developmental treatment affected which traits were plastic as adults: restricted spiders built safer webs when their adult condition increased, while ad lib spiders reduced their aggression when their adult condition increased. The amount of individual variation in behaviour and web structure varied with developmental treatment. Spiders reared on a restricted diet exhibited consistent variation in all aspects of foraging behaviour and web structure, while spiders reared on an ad lib diet exhibited consistent individual variation in aggression and web weight only. 5. Developmental experience affected the average life history, behaviour and web structure of spiders, but also shaped the amount of phenotypic variation observed among individuals. Surprisingly, developmental experience also determined the particular way in which individuals plastically adjusted their behaviour and web structure to changes in adult condition.

Multiple mating reveals complex patterns of assortative mating by personality and body size.

Understanding patterns of non-random mating is central to predicting the consequences of sexual selection. Most studies quantifying assortative mating focus on testing for correlations among partners' phenotypes in mated pairs. Few studies have distinguished between assortative mating arising from preferences for similar partners (expressed by all or a subset of the population) vs. from phenotypic segregation in the environment. Also, few studies have assessed the robustness of assortative mating against temporal changes in social conditions. We tracked multiple matings by stream water striders (Aquarius remigis) across variable social conditions to investigate mating patterns by both body size and behavioural type (personality). We documented temporal changes in partner availability and used a mixed model approach to analyse individual behaviours and changes in mating status recorded on an hourly basis. We assessed whether all or only a subset of individuals in the population expressed a tendency to mate with similar phenotypes. Our analyses took into account variation in the level of competition and in the phenotypes of available partners. Males and females exhibited significant assortative mating by body size: the largest males and females, and the smallest males and females mated together more often than random. However, individuals of intermediate size were equally likely to mate with small, intermediate or large partners. Individuals also displayed two contrasting patterns of assortative mating by personality (activity level). Individuals generally mated preferentially with partners of similar activity level. However, beyond that general trend, individuals with more extreme personalities tended to exhibit disassortative mating: the most active males mated disproportionately with less active females and the least active males tended to mate with more active females. Our analyses thus revealed multiple, distinct patterns of nonrandom mating. These mating patterns did not arise from differences in partner availability among individuals and were robust to temporal changes in social conditions. Hence, mating patterns likely reflect mate preferences or arise from male-male competition coupled with sexual conflict. Our study also stresses the importance of accounting for variation in partner availability and demonstrates the influence of behavioural variation on mating patterns.

From Individuals to Groups and Back: The Evolutionary Implications of Group Phenotypic Composition.

There is increasing interest in understanding the processes that maintain phenotypic variation in groups, populations, or communities. Recent studies have investigated how the phenotypic composition of groups or aggregations (e.g., its average phenotype or phenotypic variance) affects ecological and social processes, and how multi-level selection can drive phenotypic covariance among interacting individuals. However, we argue that these questions are rarely studied together. We present a unified framework to address this gap, and discuss how group phenotypic composition (GPC) can impact on processes ranging from individual fitness to population demography. By emphasising the breadth of topics affected, we hope to motivate more integrated empirical studies of the ecological and evolutionary implications of GPC.

Animal personality and state-behaviour feedbacks: a review and guide for empiricists.

An exciting area in behavioural ecology focuses on understanding why animals exhibit consistent among-individual differences in behaviour (animal personalities). Animal personality has been proposed to emerge as an adaptation to individual differences in state variables, leading to the question of why individuals differ consistently in state. Recent theory emphasizes the role that positive feedbacks between state and behaviour can play in producing consistent among-individual covariance between state and behaviour, hence state-dependent personality. We review the role of feedbacks in recent models of adaptive personalities, and provide guidelines for empirical testing of model assumptions and predictions. We discuss the importance of the mediating effects of ecology on these feedbacks, and provide a roadmap for including state-behaviour feedbacks in behavioural ecology research.

Pulsed resources and the coupling between life-history strategies and exploration patterns in eastern chipmunks (Tamias striatus).

Understanding the causes of animal personality (i.e. consistent behavioural differences) is a major aim of evolutionary studies. Recent theoretical work suggests that major personality traits may contribute to evolutionary trade-offs. However, such associations have only been investigated in a few study systems, and even less so in free ranging animal populations. Eastern chipmunks exhibit consistent individual differences in exploration, ranging from slow to fast. Birth cohorts also experience dramatic differences in age at first breeding opportunity due to annual differences in beech mast. Individuals may breed for the first time at 24, 33 or 50% of their average life span, depending on year of birth. Here, we used data from a long-term survey on a wild population to investigate the relationship between reproductive life history and consistent individual differences in exploration. We determined whether predictable differences in age at first breeding opportunity among birth cohorts were associated with exploration differences and favoured individuals with different exploration. Birth cohorts with a predictably earlier age at first breeding opportunity were faster explorers on average. Slower explorers displayed their highest fecundity (females) or highest fertilization success (males) later in their life compared with faster explorers. Overall, slow explorers attained a higher lifetime reproductive success than fast explorers when given an opportunity to reproduce later in their life. Our results suggest that the timing of mating seasons, associated with fluctuating food abundance, may favour individual variation in exploration and maintain population variation through its effects on reproductive life history. Together, our result shed light on how fluctuation in ecological conditions may maintain personality differences and on the nature of the relationships between animal personality and life history.

Social niche specialization under constraints: personality, social interactions and environmental heterogeneity.

Several personality traits are mainly expressed in a social context, and others, which are not restricted to a social context, can be affected by the social interactions with conspecifics. In this paper, we focus on the recently proposed hypothesis that social niche specialization (i.e. individuals in a population occupy different social roles) can explain the maintenance of individual differences in personality. We first present ecological and social niche specialization hypotheses. In particular, we show how niche specialization can be quantified and highlight the link between personality differences and social niche specialization. We then review some ecological factors (e.g. competition and environmental heterogeneity) and the social mechanisms (e.g. frequency-dependent, state-dependent and social awareness) that may be associated with the evolution of social niche specialization and personality differences. Finally, we present a conceptual model and methods to quantify the contribution of ecological factors and social mechanisms to the dynamics between personality and social roles. In doing so, we suggest a series of research objectives to help empirical advances in this research area. Throughout this paper, we highlight empirical studies of social niche specialization in mammals, where available.

Behavioural impacts of torpor expression: a transient effect in captive eastern chipmunks (Tamias striatus).

Species use torpor, an extreme form of heterothermy, to survive periods of limited resource supply. Studies of hibernating animals have shown that torpor causes major structural and physiological changes in the brain, many of which are reversed during periodic arousals. This suggests that behaviour may change during and following the hibernation period. Here we investigate individual performance in behavioural tests prior to and during hibernation by captive eastern chipmunks (Tamias striatus). Results indicate an association between deep torpor expression and atypical habituation patterns tested directly following torpor arousals. However, no association was found between torpor expression and spatial maze performance tested more than 24h post-arousal. Therefore, any behavioural impairment induced by torpor appears to be highly transient. The detected association between torpor and behaviour may be driven by previously confirmed effects of torpor on brain structure and function, though other potential covariates, such as the activation and deactivation of the stress axis, warrant consideration. Thus, our results are consistent with transient behavioural impairments following torpor arousals, but the causes and longer-term consequences of these transient impairments remain unclear.

Noninvasive monitoring of fecal cortisol metabolites in the eastern chipmunk (Tamias striatus): validation and comparison of two enzyme immunoassays.

Monitoring fecal glucocorticoid metabolites in wild animals, using enzyme immunoassays, enables the study of endocrinological patterns relevant to ecology and evolution. While some researchers use antibodies against the parent hormone (which is typically absent from fecal samples), others advocate the use of antibodies designed to detect glucocorticoid metabolites. We validated two assays to monitor fecal cortisol metabolites in the eastern chipmunk (Tamias striatus). We compared an antibody produced against cortisol and one produced against 5α-pregnane-3ß, 11ß, 21-triol-20-one using a radiometabolism study and an injection with adrenocorticotropic hormone (ACTH). Most cortisol metabolites were excreted in the urine (∼83%). Peak excretion in the feces occurred 8 h after injection. Both assays detected an increase in fecal cortisol metabolite levels after injection of ACTH. Males, but not females, exhibited a circadian variation in metabolite levels. The sexes did not exhibit any difference over the time course and route of excretion or the relative increase in fecal cortisol metabolite levels after ACTH injection. The cortisol assay displayed higher reactivity to ACTH injection relative to baseline than did the metabolite assay. While both antibodies gave comparable results, the cortisol antibody was more sensitive to changes in plasma cortisol levels in eastern chipmunks.