Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens

Research on the evolution of cooperative groups tends to explore the costs and benefits of cooperation, with less focus on the proximate behavioral changes necessary for the transition from solitary to cooperative living. However, understanding what proximate changes must occur, as well as those pre-conditions already in place, is critical to understanding the origins and evolution of sociality. The California harvester ant Pogonomyrmex californicus demonstrates population-level variation in colony founding over a close geographic range. In adjacent populations, queens either found nests as single individuals (haplometrosis) or form cooperative groups of nonrelatives (pleometrosis). We compared aggregation, aggression, and tolerance of queens from one pleometrotic and two haplometrotic populations during nest initiation, to determine which behaviors show an evolutionary shift and which are present at the transition to pleometrosis. Surprisingly, within-nest aggregative behavior was equally present among all populations. In nesting boxes with multiple available brood-rearing sites, both queen types readily formed and clustered around a single common brood pile, suggesting that innate attraction to brood (offspring) facilitates the transition to social aggregation. In contrast, queens from the three populations differed in their probabilities of attraction on the ground to nest sites occupied by other queens and in levels of aggression. Our results suggest that some key behavioral mechanisms facilitating cooperation in P. californicus are in place prior to the evolution of pleometrosis and that the switch from aggression to tolerance is critical for the evolution of stable cooperative associations.