Fine scale mapping of genomic introgressions within the Drosophila yakuba clade

The process of speciation involves populations diverging over time until they are genetically and reproductively isolated. Hybridization between nascent species was long thought to directly oppose speciation. However, the amount of interspecific genetic exchange (introgression) mediated by hybridization remains largely unknown, although recent progress in genome sequencing has made measuring introgression more tractable. A natural place to look for individuals with admixed ancestry (indicative of introgression) is in regions where species co-occur. In west Africa, D. santomea and D. yakuba hybridize on the island of São Tomé, while D. yakuba and D. teissieri hybridize on the nearby island of Bioko. In this report, we quantify the genomic extent of introgression between the three species of the Drosophila yakuba clade (D. yakuba, D. santomea), D. teissieri). We sequenced the genomes of 86 individuals from all three species. We also developed and applied a new statistical framework, using a hidden Markov approach, to identify introgression. We found that introgression has occurred between both species pairs but most introgressed segments are small (on the order of a few kilobases). After ruling out the retention of ancestral polymorphism as an explanation for these similar regions, we find that the sizes of introgressed haplotypes indicate that genetic exchange is not recent (>1,000 generations ago). We additionally show that in both cases, introgression was rarer on X chromosomes than on autosomes which is consistent with sex chromosomes playing a large role in reproductive isolation. Even though the two species pairs have stable contemporary hybrid zones, providing the opportunity for ongoing gene flow, our results indicate that genetic exchange between these species is currently rare.Author summary: Even though hybridization is thought to be pervasive among animal species, the frequency of introgression, the transfer of genetic material between species, remains largely unknown. In this report we quantify the magnitude and genomic distribution of introgression among three species of Drosophila that encompass the two known stable hybrid zones in this genetic model genus. We obtained whole genome sequences for individuals of the three species across their geographic range (including their hybrid zones) and developed a hidden Markov model-based method to identify patterns of genomic introgression between species. We found that nuclear introgression is rare between both species pairs, suggesting hybrids in nature rarely successfully backcross with parental species. Nevertheless, some D. santomea alleles introgressed into D. yakuba have spread from São Tomé to other islands in the Gulf of Guinea where D. santomea is not found. Our results indicate that in spite of contemporary hybridization between species that produces fertile hybrids, the rates of gene exchange between species are low.