Stepwise evolution of a butterfly supergene via duplication and inversion

Abstract

ABSTRACTSupergenes maintain adaptive clusters of alleles in the face of genetic mixing. Although usually attributed to inversions, there are few cases in which the specific mechanisms of recombination suppression, and their timing, have been reconstructed in detail. We investigated the origin of the BC supergene, which controls variation in warning colouration in the African Monarch butterfly, Danaus chrysippus. By generating chromosome-scale assemblies for all three alleles, we identified multiple structural differences. Most strikingly, we find that a region of >1 million bp underwent several segmental duplications at least 7.5 million years ago. The resulting duplicated fragments appear to have triggered four inversions in surrounding parts of the chromosome, resulting in stepwise growth of the region of suppressed recombination. Phylogenies for the inversions are incongruent with the species tree, and suggest that structural polymorphisms have persisted for at least 4.1 million years. In addition to the role of duplications in triggering inversions, our results suggest a previously undescribed mechanism of recombination suppression through independent losses of divergent duplicated tracts. Overall, our findings challenge the idea of instantaneous supergene evolution through a single inversion event, instead pointing towards a stepwise process involving a variety of structural changes.