Genomic islands of divergence between Drosophila yakuba subspecies predominantly overlap with chromosomal inversions

During the early stages of local adaptation and speciation, genetic differences tend to accumulate at certain regions of the genome leading to the formation of genomic islands of divergence (GIDs). This pattern may be due to selection and/or difference in the rate of recombination. Here, we investigate the possible causes of GIDs in Drosophila yakuba mayottensis, and reconfirm using field collection its association with toxic noni (Morinda citrifolia) fruits on the Mayotte island. Population genomics revealed lack of genetic structure on the island and identified 20 GIDs distinguishing D. y. mayottensis from generalist mainland populations of D. y. yakuba. The GIDs were enriched with gene families involved in the metabolism of lipids, sugars, peptides and xenobiotics, suggesting a role in host shift. We assembled a new genome for D. y. mayottensis and identified five novel chromosomal inversions. Twelve GIDs ([~]72% of outlier windows) fell close to or within subspecies-specific inversions. However, three GIDs were in collinear, high recombining regions indicating strong signal of hard selective sweeps. Unlike D. y. mayottensis, D. sechellia, the only other noni-specialist, is homosequential with its generalist relatives. Thus, both selection and rearrangements shape GIDs and striking convergences can occur between species with distinct genomic architectures.