Social dilemmas of sociality due to beneficial and costly contagion

Levels of sociality in nature vary widely. Some species are solitary; others live in family groups; some form complex multi-family societies. Increased levels of social interaction can allow for the spread of useful innovations and beneficial information, but can also facilitate the spread of harmful contagions, such as infectious diseases. It is natural to assume that these contagion processes shape the evolution of complex social systems, but an explicit account of the dynamics of sociality under selection pressure imposed by contagion remains elusive. We consider a model for the evolution of sociality strategies in the presence of both a beneficial and costly contagion. We study the dynamics of this model at three timescales: using a susceptible-infectious-susceptible (SIS) model to describe contagion spread for given sociality strategies, a replicator equation to study the changing fractions of two different levels of sociality, and an adaptive dynamics approach to study the long-time evolution of the population level of sociality. For a wide range of assumptions about the benefits and costs of infection, we identify a social dilemma: the evolutionarily-stable sociality strategy (ESS) is distinct from the collective optimum—the level of sociality that would be best for all individuals. In particular, the ESS level of social interaction is greater (respectively less) than the social optimum when the good contagion spreads more (respectively less) readily than the bad contagion. Our results shed light on how contagion shapes the evolution of social interaction, but reveals that evolution may not necessarily lead populations to social structures that are good for any or all.Author summary: Social interactions among individuals in animal groups provide a range of evolutionary benefits and risks. On the one hand, social contacts can promote learning and the adoption of innovations; on the other hand, such interactions can expose individuals to the harms of infectious disease. In this paper, we study the evolution of social gregariousness in the presence of both a beneficial and a costly contagion, which are jointly spreading in a population. Assuming that, all else equal, individuals prefer increased exposure to the good contagion and decreased exposure to the bad contagion, we characterize a socially-optimal level of gregariousness that best balances the relative exposure to the two contagions. However, using the mathematical frameworks of replicator equations and adaptive dynamics, we show that evolutionary competition between sociality strategies produces a social dilemma: individuals endeavoring to maximize their fitnesses drive the population to a level of gregariousness at which all individuals are worse off. In some cases, social behavior can disappear entirely—even when any level of gregariousness would be advantageous for the population as a whole. We also propose mechanisms to help overcome the social dilemma, showing how groups can help to establish more efficient levels of social interaction.