Genome-wide evidence for speciation with gene flow in Heliconius butterflies
Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. We have quantified admixture and genetic differentiation genome-wide at different stages of divergence in the neotropical butterfly genus Heliconius, by sequencing the whole genomes of 31 individuals. Comparisons between sympatric and allopatric populations of sister species H. melpomene and members of the H. cydno/timareta group revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100 kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Estimation of admixture at different levels of phylogenetic divergence indicated that gene flow between these species has continued since early in speciation. The level of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection on Müllerian mimicry and known Z-linked hybrid incompatibility. Overall these results show that ecologically divergent species can emerge and persist despite ongoing gene flow affecting a surprisingly large fraction of the genome.