Abstract

BackgroundProtein-coding genes expressed in sperm evolve at different rates. To gain deeper insight into the factors underlying this heterogeneity we examined the relative importance of a diverse set of previously described rate correlates in determining the evolution of murine sperm proteins.ResultsUsing partial rank correlations we detected several major rate indicators: Phyletic gene age, numbers of protein-protein interactions, and survival essentiality emerged as particularly important rate correlates in murine sperm proteins. Tissue specificity, numbers of paralogs, and untranslated region lengths also correlate significantly with sperm genes’ evolutionary rates, albeit to a lesser extent. Multifunctionality, coding sequence or average intron lengths, and mean expression level have insignificant or virtually no independent effects on evolutionary rates in murine sperm genes. Gene ontology enrichment analyses of three equally sized murine sperm protein groups classified based on their evolutionary rates indicate strongest sperm-specific functional specialization in the most quickly evolving gene class.ConclusionsWe propose a model according to which slowly evolving murine sperm proteins tend to be constrained by factors such as survival essentiality, network connectivity, and/or broad expression. In contrast, evolutionary change may arise especially in less constrained sperm proteins, which might, moreover, be prone to specialize to reproduction-related functions. Our results should be taken into account in future studies on rate variations of reproductive genes.

Highlights

  • Protein-coding genes expressed in sperm evolve at different rates

  • We compiled a set of proteins expressed in mouse epididymal sperm [40] and collected the pairwise nonsynonymous substitution rate (dN)/synonymous substitution rate (dS) estimate with rat for each coding gene as well as several variables which had previously been shown to correlate with evolutionary rates

  • The potential correlates of dN/dS comprised gene essentiality, multifunctionality, number of protein-protein interaction (PPI), expressional tissue bias (τ), mean expression level, phyletic gene age, number of paralogs, and several measures of gene compactness (CDS length, 5′ and 3′ untranslated region (UTR) length, average intron length)

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Summary

Introduction

Protein-coding genes expressed in sperm evolve at different rates. To gain deeper insight into the factors underlying this heterogeneity we examined the relative importance of a diverse set of previously described rate correlates in determining the evolution of murine sperm proteins. Different types of postmating sexual selection are thought to drive the diversification of sperm anatomy and function across taxa. It may be assumed that all proteincoding genes expressed in sperm cells could potentially experience sexual selection, adaptive evolution affects only a relatively small fraction of them. The above mentioned studies were able to partially explain rate variations of male reproductive proteins. The influence of a larger set of potential rate determinants on the evolution of mammalian sperm proteins has not yet been studied

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