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Both individual and group behavior can influence individual fitness, but multilevel selection is rarely quantified on social behaviors. Social networks provide a unique opportunity to study multilevel selection on social behaviors, as they describe complex social traits and patterns of interaction at both the individual and group levels. In this study, we used contextual analysis to measure the consequences of both individual network position and group network structure on individual fitness in experimental populations of forked fungus beetles (Bolitotherus cornutus) with two different resource distributions. We found that males with high individual connectivity (strength) and centrality (betweenness) had higher mating success. However, group network structure did not influence their mating success. Conversely, we found that individual network position had no effect on female reproductive success but that females in populations with many social interactions experienced lower reproductive success. The strength of individual-level selection in males and group-level selection in females intensified when resources were clumped together, showing that habitat structure influences multilevel selection. Individual and emergent group social behavior both influence variation in components of individual fitness, but impact the male mating success and female reproductive success differently, setting up intersexual conflicts over patterns of social interactions at multiple levels.

Social interactions with conspecifics can dramatically affect an individual’s fitness. The positive or negative consequences of interacting with social partners typically depend on the value of traits that they express. These pathways of social selection connect the traits and genes expressed in some individuals to the fitness realized by others, thereby altering the total phenotypic selection on and evolutionary response of traits across the multivariate phenotype. The downstream effects of social selection are mediated by the patterns of phenotypic assortment between focal individuals and their social partners (the interactant covariance, Cij′, or the multivariate form, CI). Depending on the sign and magnitude of the interactant covariance, the direction of social selection can be reinforced, reversed, or erased. We report estimates of Cij′ from a variety of studies of forked fungus beetles to address the largely unexplored questions of consistency and plasticity of phenotypic assortment in natural populations. We found that phenotypic assortment of male beetles based on body size or horn length was highly variable among subpopulations, but that those differences also were broadly consistent from year to year. At the same time, the strength and direction of Cij′ changed quickly in response to experimental changes in resource distribution and social properties of populations. Generally, interactant covariances were more negative in contexts in which the number of social interactions was greater in both field and experimental situations. These results suggest that patterns of phenotypic assortment could be important contributors to variability in multilevel selection through their mediation of social selection gradients.

Landscape patterns of phenotypic coevolution are determined by variation in the outcome of predator–prey interactions. These outcomes may depend not only on the functional phenotypes that mediate species interactions, but also on aspects of the environment that enable encounters between coevolutionary partners.

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Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory and, in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates.

Antagonistic coevolution between natural enemies can produce highly exaggerated traits, such as prey toxins and predator resistance. This reciprocal process of adaptation and counter‐adaptation may also open doors to other evolutionary novelties not directly involved in the phenotypic interface of coevolution. We tested the hypothesis that predator–prey coevolution coincided with the evolution of conspicuous coloration on resistant predators that retain prey toxins. In western North America, common garter snakes (Thamnophis sirtalis) have evolved extreme resistance to tetrodotoxin (TTX) in the coevolutionary arms race with their deadly prey, Pacific newts (Tarichaspp.). TTX‐resistant snakes can retain large amounts of ingested TTX, which could serve as a deterrent against the snakes' own predators if TTX toxicity and resistance are coupled with a conspicuous warning signal. We evaluated whether arms race escalation covaries with bright red coloration in snake populations across the geographic mosaic of coevolution. Snake colour variation departs from the neutral expectations of population genetic structure and covaries with escalating clines of newt TTX and snake resistance at two coevolutionary hotspots. In the Pacific Northwest, bright red coloration fits an expected pattern of an aposematic warning to avian predators: TTX‐resistant snakes that consume highly toxic newts also have relatively large, reddish‐orange dorsal blotches. Snake coloration also seems to have evolved with the arms race in California, but overall patterns are less intuitively consistent with aposematism. These results suggest that interactions with additional trophic levels can generate novel traits as a cascading consequence of arms race coevolution across the geographic mosaic.

Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of “trait remixing” in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.

Intrasexual interactions can determine which individuals within a population have access to limited resources. Despite their potential importance on fitness generally and mating success especially, female–female interactions are not often measured in the same species where male–male interactions are well‐defined. In this study, we characterized female–female interactions inBolitotherus cornutus, a mycophagous beetle species native to Northeastern North America. We used dyadic, behavioral assays to determine whether females perform directly aggressive or indirectly exclusionary competitive behaviors. Polypore shelf fungus, an important food and egg‐laying resource forB.cornutusfemales, is patchily distributed and of variable quality, so we tested for competition over fungus as a resource. Behavior of females was assessed in three sets of dyadic trials with randomly paired female partners. Overall, females did not behave aggressively toward their female partner or perform exclusionary behaviors over the fungal resource. None of the behaviors performed by females were individually repeatable. Two scenarios may explain our lack of observed competition: our trial context may not induce competition, or femaleB.cornutussimply may not behave competitively in the wild. We compare our results to a similar study on male–male interactions in the same species and propose future studies on female–female interactions under different competitive contexts to expand the understanding of female competition.

Social interactions drive many important ecological and evolutionary processes. It is therefore essential to understand the intrinsic and extrinsic factors that underlie social patterns. A central tenet of the field of behavioural ecology is the expectation that the distribution of resources shapes patterns of social interactions.

Females must choose among potential mates with different phenotypes in a variety of social contexts. Many male traits are inherent and unchanging, but others are labile to social context. Competition, for example, can cause physiological changes that reflect recent wins and losses that fluctuate throughout time. We may expect females to respond differently to males depending on the outcome of their most recent fight. InBolitotherus cornutus(forked fungus beetles), males compete for access to females, but copulation requires female cooperation. In this study, we use behavioral trials to determine whether females use chemical cues to differentiate between males and whether the outcome of recent male competition alters female preference. We measured female association time with chemical cues of two size‐matched males both before and after male–male competition. Females in our study preferred to associate with future losers before males interacted, but changed their preference for realized winners following male competitive interactions. Our study provides the first evidence of change in female preference based solely on the outcome of male–male competition.