Adaptive Introgression across Species Boundaries in Heliconius Butterflies

Abstract

It is widely documented that hybridisation occurs between many closely related species, but the importance of introgression in adaptive evolution remains unclear, especially in animals. Here, we have examined the role of introgressive hybridisation in transferring adaptations between mimetic Heliconius butterflies, taking advantage of the recent identification of a gene regulating red wing patterns in this genus. By sequencing regions both linked and unlinked to the red colour locus, we found a region that displays an almost perfect genotype by phenotype association across four species, H. melpomene, H. cydno, H. timareta, and H. heurippa. This particular segment is located 70 kb downstream of the red colour specification gene optix, and coalescent analysis indicates repeated introgression of adaptive alleles from H. melpomene into the H. cydno species clade. Our analytical methods complement recent genome scale data for the same region and suggest adaptive introgression has a crucial role in generating adaptive wing colour diversity in this group of butterflies.

Author Summary

Hybridisation occurs between many animal species, however its evolutionary relevance is still a matter of great debate. While some argue that hybridisation leads to maladaptive gene combinations, and therefore to an evolutionary dead end, others consider interspecific hybridisation as a process with great potential to fuel evolution. We examine this question by exploring the origins of red wing colouration, a trait under natural selection, in the adaptive radiation of closely related species of Heliconius butterflies. By sequencing genetic regions both linked and unlinked to the red wing pattern locus, we found experimental evidence supporting multiple hybridisation events that have mediated the acquisition of colour adaptations from H. melpomene to H. timareta. This introgression has allowed H. timareta to colonise new fitness peaks in the Müllerian mimicry landscape. In this way, our results support the idea that interspecific hybridisation in animals constitutes a source of genetic variation that promotes diversification.