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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.

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.