Supergene evolution triggered by the introgression of a chromosomal inversion

Abstract

Supergenes are groups of tightly linked loci whose variation is inherited as a single Mendelian locus and are a common genetic architecture for complex traits under balancing selection1. Supergene alleles are long-range haplotypes with numerous mutations underlying distinct adaptive strategies, often maintained in linkage disequilibrium through the suppression of recombination by chromosomal rearrangements2-5. However, the mechanism governing the formation of supergenes is not well understood, and poses the paradox of establishing divergent functional haplotypes in face of recombination1,6. Here, we show that the formation of the supergene alleles encoding mimicry polymorphism in the butterfly Heliconius numata is associated with the introgression of a divergent, inverted chromosomal segment. Haplotype divergence and linkage disequilibrium indicate that supergene alleles, each allowing precise wing-pattern resemblance to distinct butterfly models, originate from over a million years of independent chromosomal evolution in separate lineages. These \"superalleles\" have evolved from a chromosomal inversion captured by introgression and maintained in balanced polymorphism, triggering supergene inheritance. This mode of evolution is likely to be a common feature of complex structural polymorphisms associated with the coexistence of distinct adaptive syndromes, and shows that the reticulation of genealogies may have a powerful influence on the evolution of genetic architectures in nature.