Recombination rate variation shapes barriers to introgression across butterfly genomes

Abstract

Hybridisation and introgression can dramatically alter the relationships among groups of species, leading to phylogenetic discordance across the genome and between populations. Introgression can also erode species differences over time, but selection against introgression at certain loci acts to maintain postmating species barriers. Theory predicts that species barriers made up of many loci throughout the genome should lead to a broad correlation between introgression and recombination rate, which determines the extent to which selection on deleterious foreign alleles will affect neutral alleles at physically linked loci. Here, we describe the variation in genealogical relationships across the genome among three species of Heliconius butterflies: H. melpomene ( mel), H. cydno ( cyd), and H. timareta ( tim), using whole genomes of 92 individuals, and ask whether this variation can be explained by heterogeneous barriers to introgression. We find that species relationships vary predictably at the chromosomal scale. By quantifying recombination rate and admixture proportions, we then show that rates of introgression are predicted by variation in recombination rate. This implies that species barriers are highly polygenic, with selection acting against introgressed alleles across most of the genome. In addition, long chromosomes, which have lower recombination rates, produce stronger barriers on average than short chromosomes. Finally, we find a consistent difference between two species pairs on either side of the Andes, which suggests differences in the architecture of the species barriers. Our findings illustrate how the combined effects of hybridisation, recombination, and natural selection, acting at multitudes of loci over long periods, can dramatically sculpt the phylogenetic relationships among species.

Author summary

Many species occasionally hybridise and share genetic material with related species. Interspecific gene flow may be counteracted by natural selection at particular ‘barrier loci’. As a result, a pair of species can end up sharing more genetic variation in some parts of their genome than in others, and the tree of relationships in a group of species can differ from one part of the genome to another. We studied relationships and barriers among three species of Heliconius butterflies using whole-genome sequences from nine populations. We find that species relationships vary dramatically and predictably across the genome because the species barriers are more porous in genomic regions with higher recombination rates. This occurs because recombination determines how broadly the surrounding genome is affected by a barrier locus. The genome-wide pattern suggests that barrier loci are widespread across the genome. One consequence is that smaller chromosomes, which have higher recombination rates, tend to have weaker species barriers than longer chromosomes. The relationships among populations on small chromosomes therefore tend to be predicted by geography, rather than by which species they belong to. Our work shows how hybridisation, recombination, and selection interact to reshape species’ relationships.