Multiple origins of a sex ratio supergene in Formica ants

Polymorphisms in complex traits often map to regions of the genome with two or more functional mutations with little or no recombination between them. These “supergenes” are usually found in a single species or a few closely related species. However, when supergenes persist through a large number of speciation events, they may take on additional functions in different lineages. Here, we investigate how an ancient supergene has evolved to gain novel function. In Formica ants, most species have a “social” supergene with M and P haplotypes that determine whether a colony is headed by a single queen or multiple queens, respectively, and which diverged from each other at least 20 million years ago. At least three Formica species have an additional haplotype on the same chromosome, termed MD, associated with female-biased offspring sex ratio at the colony level. Do the MD haplotypes share a common origin or did they evolve convergently? With whole-genome resequencing, we identify MD haplotypes in three additional species and use variation across six Formica species to examine the evolutionary history of the MD haplotype. We identify two putative origins of the MD haplotype, one in the ancestor of five Nearctic species, and a second in the Palearctic species F. cinerea. We present evidence that the MD haplotypes originated from recombination between M and P haplotypes. The discovery of two MD haplotypes convergently evolving from distinct recombination events between two ancestral supergene haplotypes illustrates how supergenes can diversify and gain additional phenotypes.