Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins

Abstract

To assess the relative impact of functional constraint and post-mating sexual selection on sequence evolution of reproductive proteins, we examined 169 primate sperm proteins. In order to recognize potential genome-wide trends, we additionally analysed a sample of altogether 318 non-reproductive (brain and postsynaptic) proteins. Based on cDNAs of eight primate species (Anthropoidea), we observed that pre-mating sperm proteins engaged in sperm composition and assembly show significantly lower incidence of site-specific positive selection and overall lower non-synonymous to synonymous substitution rates (dN/dS) across sites as compared with post-mating sperm proteins involved in capacitation, hyperactivation, acrosome reaction and fertilization. Moreover, database screening revealed overall more intracellular protein interaction partners in pre-mating than in post-mating sperm proteins. Finally, post-mating sperm proteins evolved at significantly higher evolutionary rates than pre-mating sperm and non-reproductive proteins on the branches to multi-male breeding species, while no such increase was observed on the branches to unimale and monogamous species. We conclude that less protein–protein interactions of post-mating sperm proteins account for lowered functional constraint, allowing for stronger impact of post-mating sexual selection, while the opposite holds true for pre-mating sperm proteins. This pattern is particularly strong in multi-male breeding species showing high female promiscuity.

Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions

“…The results of these studies are, however, mixed. Some SFP genes show clearly elevated rates of amino acid substitution in species in which females mate with many males (polyandry); however, many SFP loci do not show this pattern (reviewed in Wong 2011; see also Claw 2013; Schumacher et al 2014). The reason for this inconsistency could be that the strength of selection may not be consistent for the same SFP across multiple species, perhaps because different signals and pathways may operate in different lineages.…”

Nonfertilizing sperm in Lepidoptera show little evidence for recurrent positive selection

“…Yet there are also many instances of reproductive proteins that diverge quickly because of relaxed purifying selection owing to expression in a single sex instead of the whole population (Barker, Demuth, & Wade, ; Wade, Priest, & Cruickshank, ). Many other factors, including number of protein‐protein interactions or importance of reproductive role, can also act to shape the intensity of positive or purifying selection on reproductive proteins (Schumacher, Rosenkranz, & Herlyn, ; Schumacher, Zischler, & Herlyn, ). Recent theoretical work has formalized the prediction that strong purifying selection on sperm proteins should depend on high rates of polyandry to generate sperm competition (Dapper & Wade, ).…”

“…Many other factors, including number of protein-protein interactions or importance of reproductive role, can also act to shape the intensity of positive or purifying selection on reproductive proteins (Schumacher, Rosenkranz, & Herlyn, 2014;Schumacher, Zischler, & Herlyn, 2017). Recent theoretical work has formalized the prediction that strong purifying selection on sperm proteins should depend on high rates of polyandry to generate sperm competition (Dapper & Wade, 2016).…”

Intra-Protein Coevolution Is Increasingly Functional with Greater Proximity to Fertilization

“…Numerous male reproductive proteins show elevated rates of sequence evolution [e.g., Torgerson et al, 2002;Clark and Swanson, 2005;Haerty et al, 2007]. The probable driving force behind is commonly seen in the various forms of postcopulatory sexual selection, including sperm competition [e.g., Lüke et al, 2014;Ramm et al, 2014;Schumacher et al, 2014], cryptic female choice [Gasparini and Pilastro, 2011;Løvlie et al, 2013], and sexual conflict Sirot et al, 2014]. Prominent examples of male reproductive genes under postcopulatory sexual selection are primate and rodent protamines and semenogelins, whereby the first replace histones in the sperm head [Wyckoff et al, 2000;Ramm et al, 2008;Lüke et al, 2014] and the latter polymerize to a copulation plug in the female genital tract [Jensen-Seaman and Li, 2003;Dorus et al, 2004;Ramm et al, 2008].…”

“…In fact, the closer male reproductive proteins are functionally related to fertilization, the higher seems to be their rate of sequence evolution. In contrast, proteins expressed in the male reproductive tract show considerable sequence conservation when they are only indirectly involved in reproduction [Dean et al, 2009;Ramm et al, 2009;Dorus et al, 2010;Schumacher et al, 2014].…”