Positive selection in the adhesion domain of Mus sperm Adam genes through gene duplications and function-driven gene...

Sperm and testes-expressed Adam genes have been shown to undergo bouts of positive selection in mammals. Despite the pervasiveness of positive selection signals, it is unclear what has driven such selective bouts. The fact that only sperm surface Adam genes show signals of positive selection within their adhesion domain has led to speculation that selection might be driven by species-specific adaptations to fertilization or sperm competition. Alternatively, duplications and neofunctionalization of Adam sperm surface genes, particularly as it is now understood in rodents, might have contributed to an acceleration of evolutionary rates and possibly adaptive diversification.

Here we sequenced and conducted tests of selection within the adhesion domain of sixteen known sperm-surface Adam genes among five species of the Mus genus. We find evidence of positive selection associated with all six Adam genes known to interact to form functional complexes on Mus sperm. A subset of these complex-forming sperm genes also displayed accelerated branch evolution with Adam5 evolving under positive selection. In contrast to our previous findings in primates, selective bouts within Mus sperm Adams showed no associations to proxies of sperm competition. Expanded phylogenetic analysis including sequence data from other placental mammals allowed us to uncover ancient and recent episodes of adaptive evolution.

The prevailing signals of rapid divergence and positive selection detected within the adhesion domain of interacting sperm Adams is driven by duplications and potential neofunctionalizations that are in some cases ancient (Adams 2, 3 and 5) or more recent (Adams 1b, 4b and 6).