Genomic evidence of a complex supergene system linking dispersal to social polymorphism

Supergenes play an important role in the evolution of complex phenotypes, locking specific combinations of alleles. One of such complex phenotypes is social polymorphism in ants, i.e., the presence of single (monogyne) or multiple (polygyne) reproductive queens within colonies, known to be determined by a social supergene in at least five species. It is associated with divergent individual and colonial traits, some linked to dispersal. We explored the idea that antagonist selection between social forms favours the emergence of regions of suppressed recombination. To this end, we studied the ant Myrmecina graminicola, in which a social polymorphism is coupled with the presence/absence of wings in queens. We discovered a new “social supergene” of ~20 Mb with three haplotypes, whose genotypic combination determines the three phenotypes observed in nature, the monogyne winged, monogyne apterous and polygyne apterous queens. The two haplotypes associated with aptery carry an additional copy of a gene probably involved in wing development as part of a ~116 kb insertion predating the origin of the social supergene (~20Mya vs. ~1Mya). Syntenic analyses showcased an independent evolution of the social supergene. The screening of workers' genotypes suggests that assortative mating and selfish behaviours may play a role in preserving supergene polymorphism. This unique supergene system illustrates the theoretically expected genetic link between social polymorphism and dispersal in ants. Its modular evolution mirrors the role of sexually antagonistic selection in the origin of sex chromosomes and makes ants a very promising model for studying supergene evolution.