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.
Highlights
Sexual selection is well known for driving the evolution of diverse male traits in a wide range of taxa, including genital morphology in insects [1], coloration in cichlids [2] as well as sperm mid-piece length and testis size in primates [3,4]
We assessed levels of functional constraint for each of the 169 sperm proteins based on numbers of direct and indirect protein– protein interaction partners (PIP) as taken from 17 out of 25 databases available through PSICQUIC (Proteomics Standard Initiative Common QUery InterfaCe; state 27 May 2013), using human protein IDs as search items and employing the PSICQUIC clustering feature that provides a non-redundant list of interactants
Our data suggest that less functional constraint and more effective post-mating sexual selection explain overall increased nonsynonymous/synonymous substitution rate ratios in postmating relative to pre-mating sperm proteins
Summary
Sexual selection is well known for driving the evolution of diverse male traits in a wide range of taxa, including genital morphology in insects [1], coloration in cichlids [2] as well as sperm mid-piece length and testis size in primates [3,4]. Whenever short branches impaired the inference of dN/dS estimates for at least one of the terminal branches or foregrounds compared, a protein was excluded from downstream analyses This procedure led to inclusion of 29 pre-mating sperm, 25 post-mating sperm and 102 non-reproductive proteins when focusing on the branches to common chimpanzee and northern white-cheeked gibbon (see the electronic supplementary material, tables S7, S8 and S10). We assessed levels of functional constraint for each of the 169 sperm proteins based on numbers of direct and indirect protein– protein interaction partners (PIP) as taken from 17 out of 25 databases available through PSICQUIC (Proteomics Standard Initiative Common QUery InterfaCe; state 27 May 2013), using human protein IDs as search items (see the electronic supplementary material, tables S1 and S2) and employing the PSICQUIC clustering feature that provides a non-redundant list of interactants. Accession numbers of cDNAs and data on sequence analyses and nPIP are reported in the electronic supplementary material, tables S9 and S10
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