Repeated evolution of supergenes on an ancient social chromosome

Supergenes are non-recombining chromosomal regions that code for complex polymorphic traits. Advances in population genomics have uncovered supergenes associated with diverse traits, ranging 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 (monogyne) or multiple queens (polygyne) colonies. We discovered a new supergene associated with similar polymorphism in the desert ant Cataglyphis niger . Despite Cataglyphis being more closely related to Formica than Solenopsis , its social chromosome is homologous to that of Solenopsis , with conservation of synteny in gene content and order. This suggests that the social chromosome is ancient, dating back to the common ancestor of Solenopsis and Cataglyphis , at least 90 million years ago. Previous work dated the Solenopsis supergene to be only one million years old, therefore, we propose that the two supergenes evolved independently in the two diverged lineages on this ancient social chromosome. Comparative analysis of hymenopteran genomes further revealed a bee chromosome homologous to the ants’ social chromosome. The conservation of the gene set on these homologous chromosomes in ants and bees suggests that this chromosome plays an important role in social behavior 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.