A comprehensive evolutionary scenario for the origin and neofunctionalization of theDrosophilaspeciation geneOdysseus(OdsH)

Author:

Vilas Boas Nunes WilliamORCID,Siqueira de Oliveira DanielORCID,de Rezende Dias Guilherme,Carvalho Antonio BernardoORCID,Putinhon Ícaro CarusoORCID,Matos Biselli JoiceORCID,Guegen Nathalie,Akkouche AbdouORCID,Burlet NellyORCID,Vieira CristinaORCID,Carareto Claudia M. A.ORCID

Abstract

AbstractOdysseus(OdsH) was the first gene described inDrosophilarelated to speciation and hybrid sterility. This gene was first described in themelanogastersubgroup and more specifically in the sterile hybrids from crosses betweenD. mauritianaandD. simulans. Its origin is attributed to the duplication of the geneunc-4, which would have occurred in the ancestor of the subgenusSophophora. By using a much larger sample ofDrosophilaspecies, we showed that contrary to what has been previously proposed,OdsHorigin occurred approximately 62 million years ago (Mya). Then,OdsHhave 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 ofD. mauritianathat could result in incompatibility with genomes from other species. We then explored the expression ofOdsHin the spermatocytes ofD. arizonaeandD. mojavensis, a pair of recently diverged sister species with incomplete reproductive isolation and expected to find the involvement ofOdsHin hybrid sterility. Our data indicated thatOdsHexpression is not atypical in male-sterile hybrids from these species. In conclusion, we have demonstrated that the origin ofOdsHoccurred 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 themelanogastersubgroup of species, may be restricted to this specific taxon.

Publisher

Cold Spring Harbor Laboratory

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