Frequency-dependent selection of a recently derived social parasite in the clonal raider ant
Waring Trible, Waring Trible , Angelina Limon , Daniel Kronauer
Late; Laboratory of Social Evolution and Behavior, The Rockefeller University, USA ; Laboratory of Social Evolution and Behavior, The Rockefeller University, USA ; Laboratory of Social Evolution and Behavior, The Rockefeller University, USA
Many ant species are host to inquiline social parasites, genetic lineages with constitutively queen-like morphology that exploit closely related wild-type colonies. Here we describe a recently derived socially parasitic lineage in the clonal raider ant, Ooceraea biroi. These parasites possess a host of heritable phenotypic differences from wild-types, including aberrant queen-like development of the ovaries and wings. The parasites lay eggs at a higher rate than wild-types, but this fitness boost is balanced by an elevated mortality during eclosion that increases as the parasites become more common within a colony. This parasitic lineage is therefore under negative frequency-dependent selection, allowing them to stably exist in wild-type colonies without going extinct or going to fixation. In contrast to the complexity of the mutant phenotype, microsatellites and whole-genome resequencing indicate that the parasites are derived from one of the previously described clone lines of O. biroi, and differ from wild-types at a small number of loci genome-wide. It is therefore likely that one or a few highly pleiotropic mutations gave rise to the parasitic phenotype. This conclusion, if true, would be relatively surprising in the context of classical evolutionary theory, in which pleiotropic mutations are expected to impede adaptive evolution because rare positive phenotypic effects are accompanied by more common negative effects. We propose that pleiotropic mutations may actually facilitate the evolution of certain kinds of adaptive phenotypes, such as the recurrent origin of inquiline social parasites in ants.