Population genomics supports multiple hybrid zone origins of socially hybridogenetic lineages of Pogonomyrmex harvester ants.

Reproductive division of labor in the social insects is typically determined by environmental cues; however, genetic effects on caste have been discovered in a growing set of ant taxa. An extreme form of genetic caste determination is "social hybridogenesis," in which co-occurring genetic lineages obligately interbreed to produce workers, whereas daughter queens are of pure-lineage ancestry. In this study, we tested the hypothesis that social hybridogenesis in the genus Pogonomyrmex resulted from one or more interspecific hybridization events, and if so, whether individual lineages were of hybrid ancestry. We reconstructed evolutionary relationships of four lineage pairs to populations of two closely related non-hybridogenetic species, Pogonomyrmex barbatus and Pogonomyrmex rugosus, using nuclear SNP loci and mitochondrial sequencing. The nuclear phylogeny supported a hybridization hypothesis, with one member of each pair nested within P. rugosus, whereas the other was nested within P. barbatus. The source populations corresponded with two distinct geographic areas at the eastern and western edges of a zone of contact. Relatively little gene flow was detected between interbreeding lineages, either historically or currently. This suggests that shifts in reproductive caste determination may reinforce reproductive incompatibility, in a manner similar to the evolution of hybridogenesis in nonsocial systems.