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.^1,2,3 One such complex phenotype is social polymorphism in ants, i.e., the presence of single (monogyne) or multiple (polygyne) reproductive queens within colonies, known to be determined by social supergenes in at least five lineages.^4,5 This polymorphism is associated with divergent individual and colonial traits, some linked to dispersal.⁶ We explored the idea that antagonistic selection between social forms favors 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. Supergene genotypes determine the three queen phenotypes observed in nature: monogyne winged, monogyne apterous, and polygyne apterous. 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 (∼20 vs. ∼1 mya). Syntenic analyses showcased an independent evolution of the social supergene. The screening of workers' genotypes suggests that assortative mating and segregation distortion 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.