Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group

Abstract

Studies of gene flow between recently diverged species can illuminate the role of natural selection in the formation of new species. Drosophila santomea and D. yakuba are recently diverged, partially reproductively isolated species that continue to hybridize in the wild, and appear to be reproductively isolated from the more distantly related species D. teissieri. We examine patterns of nucleotide polymorphism and divergence in these three species at multiple X-linked, Y-linked, and mitochondrial markers. All three species harbor drastically reduced variability on the Y chromosome relative to the X, as expected for a nonrecombining chromosome subject to variation-reducing selection. The three species are generally well differentiated at the nuclear markers, with little evidence for recent introgression for either the X- or Y-linked genes. Based on the nuclear genes, we estimate that D. santomea and D. yakuba diverged about one-half million years ago and split from D. teissieri about one million years ago. In contrast to the pattern at nuclear loci, all three species share a very similar mtDNA haplotype. We show that the mtDNA must have recently introgressed across species boundaries in the D. yakuba subgroup and that its fixation was driven by either selection on the mitochondria itself or other cytoplasmic factors. These results demonstrate that different regions of the genome can have distinct evolutionary dynamics in the context of species formation. Although natural selection is usually thought of as accentuating divergence between species, our results imply that it can also act as a homogenizing force.