A comprehensive evolutionary scenario for the origin and neofunctionalization of the Drosophila speciation gene Odysseus (OdsH)

Odysseus (OdsH) was the first gene described in Drosophila related to speciation and hybrid sterility. This gene was first described in the melanogaster subgroup and more specifically in the sterile hybrids from crosses between D. mauritiana and D. simulans. Its origin is attributed to the duplication of the gene unc-4, which would have occurred in the ancestor of the subgenus Sophophora. By using a much larger sample of Drosophila species, we showed that contrary to what has been previously proposed, OdsH origin occurred approximately 62 million years ago (Mya). Then, OdsH have experienced rapid neofunctionalization in male reproductive tracts, evidenced by its evolutionary rates, expression and transcription factor binding sites. Furthermore, the analysis of the OdsH peptide sequence allowed the identification of mutations in the DNA- and protein-binding domains of D. mauritiana that could result in incompatibility with genomes from other species. We then explored the expression of OdsH in the spermatocytes of D. arizonae and D. mojavensis, a pair of recently diverged sister species with incomplete reproductive isolation and expected to find the involvement of OdsH in hybrid sterility. Our data indicated that OdsH expression is not atypical in male-sterile hybrids from these species. In conclusion, we have demonstrated that the origin of OdsH occurred earlier than previously proposed and that its neofunctionalization in male sexual functions occurred rapidly after its origin. Our results also suggested that its role as a speciation gene, as in the melanogaster subgroup of species, may be restricted to this specific taxon.