Repeated evolution of supergenes on an ancient social chromosome

Supergenes are non-recombining chromosomal regions that encode complex polymorphic traits. Advances in population genomics have uncovered supergenes associated with diverse traits, from butterfly wing patterns to floral morphs. In ants, two supergenes on non-homologous "social chromosomes" in Solenopsis and Formica are associated with social polymorphism, with either single-queen or multiple-queen colonies. We discovered a new supergene associated with a similar polymorphism in the desert ant Cataglyphis niger. Despite Cataglyphis being more closely related to Formica, its social chromosome is homologous to Solenopsis, with conservation of synteny in gene content and order. This suggests that the chromosome is ancient, dating back to the common ancestor of Solenopsis and Cataglyphis at least 90 million years ago. Low sequence divergence between supergene haplotypes in both Solenopsis and Cataglyphis suggests that the two supergenes evolved recently and independently in the two divergent lineages on this ancient social chromosome. Comparative analysis of hymenopteran genomes further revealed a bee chromosome homologous to the ants' social chromosome. This chromosome contains the largest set of genes conserved as a linkage group across ants and bees. The conserved gene set is enriched for olfactory functions, notably numerous odorant-binding proteins. The conservation of this gene set suggests that this chromosome plays an important role in sociobiology across social Hymenoptera. We propose that the conserved gene set in the social chromosome was repeatedly used as a pre-adapted toolkit for the evolution of social traits in general and specifically in the evolution of polygyne social structure in ants.