Social dynamics drive selection in cooperative associations of ant queens

Social dynamics, the emergent effects of interactions within structured groups, play a key role in shaping social phenotypes and fitness. We examined the potential positive and negative effects of social dynamics in simple groups, by creating social groups of harvester ant queens with 2 alternate nest-founding strategies, solitary versus cooperative. We compared social interactions, survival, and nest productivity of pairs containing queens from the cooperative founding population, the normally solitary founding population, or mixed pairs of the 2 types. Expressed social phenotypes of queens in pairs depended strongly on the lineage of the other queen. Two behaviors, aggression and brood care, showed simple social dynamical effects. Aggression escalated in pairs of normally solitary queens, whereas queens in cooperative pairs coordinated brood output, leading to more efficient worker production. These dynamics had context-based fitness consequences, such that cooperative queens gained a survival advantage in cooperative pairs, but neither type of queen experienced an advantage or disadvantage in mixed associations. The interplay between social dynamics and fitness in these associations provides an empirical example of social selection. It captures a likely scenario of the transition to and the early evolution of cooperative living, in which cooperative individuals interact with solitary individuals who lack a priori strategies for cooperation or cheating.