The Foundress' Dilemma: Group selection for cooperation among queens of Pogonomyrmex californicus

The evolution of cooperation is a fundamental problem in biology, especially in cases where inclusive fitness benefits from relatedness cannot counter potential within-group inequalities in fitness. With his “haystack” model, Maynard Smith captured this tension between individual and group fitness via the assumption that cooperation generates a competitive advantage at the group level, but cooperators may be at a local disadvantage within their social group. These assumptions allowed the possibility of group selection, but under conditions thought unlikely to be found in natural populations. Here we show that a haystack-like model can explain the evolution of a cooperative nest founding phenotype in the harvester ant Pogonomyrmex californicus. Through most of this species’ range, new colonies are founded by single queens, but in some populations nests are instead founded by cooperative groups of queens.  In mixed groups of cooperative and single-founding (non-cooperative) queens, we found that the latter survived longer than their cooperative nestmates, but that foundress groups with non-cooperators died out entirely more often than those with only cooperative members. An agent-based model shows that the between-group advantage of the cooperative phenotype allows it go to fixation, despite its within-group disadvantage, but only at sufficiently high population densities; a context where between-group competition becomes more intense. Supporting field data show a higher nest density in the population where cooperative founding is common, consistent with greater density driving the evolution of cooperative colony foundation through selection at the group level. This is the first demonstration of group selection for cooperative behavior among unrelated animals in a natural setting.