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.
Social group structure is highly variable and can be important for nearly every aspect of behavior and its fitness consequences. Group structure can be modeled using social network analysis, but we know little about the evolutionary factors shaping and maintaining variation in how individuals are embedded within their networks (i.e., network position). While network position is a pervasive target of selection, it remains unclear whether network position is heritable and can respond to selection. Furthermore, it is unclear how environmental factors interact with genotypic effects on network positions, or how environmental factors shape selection on heritable network structure. Here we show multiple measures of social network position are heritable, using replicate genotypes and replicate social groups of Drosophila melanogaster flies. Our results indicate genotypic differences in network position are largely robust to changes in the environment flies experience, though some measures of network position do vary across environments. We also show selection on multiple network position metrics depends on the environmental context they are expressed in, laying the groundwork for better understanding how spatio-temporal variation in selection contributes to the evolution of variable social group structure.
Oviposition site decisions often maximize offspring fitness, but costs constraining choice can cause females to oviposit in poor developmental environments. It is unclear whether these constraints cumulatively outweigh offspring fitness to determine oviposition decisions in wild populations. Understanding how constraints shape oviposition in natural landscapes is a critical step toward revealing how maternal behavior influences fundamental phenomena like the evolution of specialization and the use of sink environments. Here, we used a genetic capture-recapture technique to reconstruct the oviposition decisions of individual females in a natural metapopulation of a beetle (Bolitotherus cornutus) that oviposits on three fungus species. We measured larval fitness-related traits (mass, development time, survival) on each fungus and compared the oviposition preferences of females in laboratory versus field tests. Larval fitness differed substantially among fungi, and females preferred a high-quality (high larval fitness) fungus in laboratory trials. However, females frequently laid eggs on the lowest-quality fungus in the wild. They preferred high-quality fungi when moving between oviposition sites, but this preference disappeared as the distance between sites increased and was inconsistent between study plots. Our results suggest that constraints on oviposition preferences in natural landscapes are sufficiently large to drive oviposition in poor developmental environments even when offspring fitness consequences are severe.
Fluctuating environmental pressures can challenge organisms by repeatedly shifting the optimum phenotype. Two contrasting evolutionary strategies to cope with these fluctuations are 1) evolution of the mean phenotype to follow the optimum (adaptive tracking) or 2) diversifying phenotypes so that at least some individuals have high fitness in the current fluctuation (bet-hedging). Bet-hedging could underlie stable differences in the behavior of individuals that are present even when genotype and environment are held constant. Instead of being simply ‘noise,’ behavioral variation across individuals may reflect an evolutionary strategy of phenotype diversification. Using geographically diverse wild-derived fly strains and high-throughput assays of individual preference, we tested whether thermal preference variation in Drosophila melanogaster could reflect a bet-hedging strategy. We also looked for evidence that populations from different regions differentially adopt bet-hedging or adaptive-tracking strategies. Computational modeling predicted regional differences in the relative advantage of bet-hedging, and we found patterns consistent with that in regional variation in thermal preference heritability. In addition, we found that temporal patterns in mean preference support bet-hedging predictions and that there is a genetic basis for thermal preference variability. Our empirical results point to bet-hedging in thermal preference as a potentially important evolutionary strategy in wild populations.
The position an individual holds in a social network is dependent on both its direct and indirect social interactions. Because social network position is dependent on the actions and interactions of conspecifics, it is likely that the genotypic composition of individuals within a social group impacts individuals' network positions. However, we know very little about whether social network positions have a genetic basis, and even less about how the genotypic makeup of a social group impacts network positions and structure. With ample evidence indicating that network positions influence various fitness metrics, studying how direct and indirect genetic effects shape network positions is crucial for furthering our understanding of how the social environment can respond to selection and evolve. Using replicate genotypes of Drosophila melanogaster fruit flies, we created social groups that varied in their genotypic makeup. Social groups were videoed, and networks were generated using motion-tracking software. We found that both an individual's own genotype and the genotypes of conspecifics in its social group affect its position within a social network. These findings provide an early example of how indirect genetic effects and social network theory can be linked, and shed new light on how quantitative genetic variation shapes the structure of social groups. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
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