Convergent evolution of social hybridogenesis in Messor harvester ants

Sexual reproduction generally requires no more than two partners. Here, we show convergent evolution of social hybridogenesis, a reproductive system requiring three reproductive partners in harvester ants. In this unorthodox reproductive system, two distinct genetic lineages live in sympatry and queens have to mate with males of their own lineage to produce queens along with males of the alternative lineage to produce workers. Using a large transcriptomic data set of nine species, we show that social hybridogenesis evolved at least three times independently in the genus Messor. Moreover, a study of 13 populations of Messor barbarus revealed that this mode of reproduction is fixed in the whole range of this ecologically dominant species. Finally, we show that workers can produce males carrying genes of the two genetic lineages, raising the possibility of rare gene flow between lineages contributing to the long-term maintenance of pairs of interdependent lineages. These results emphasize the evolutionary importance of social hybridogenesis, a major transition possibly linked to the peculiar ecology of harvester ants.