Abstract

Most genes linked to male reproductive function have been known to evolve rapidly among species and to show signatures of positive selection. Different male species-specific reproductive strategies have been proposed to underlie positive selection, such as sperm competitive advantage and control over females postmating physiology. However, an underexplored aspect potentially affecting male reproductive gene evolution in mammals is the effect of gene duplications. Here we analyze the molecular evolution of members of the izumo gene family in mammals, a family of four genes mostly expressed in the sperm with known and potential roles in sperm-egg fusion. We confirm a previously reported bout of selection for izumo1 and establish that the bout of selection is restricted to the diversification of species of the superorder Laurasiatheria. None of the izumo genes showed evidence of positive selection in Glires (Rodentia and Lagomorpha), and in the case of the non-testes-specific izumo4, rapid evolution was driven by relaxed selection. We detected evidence of positive selection for izumo3 among Primates. Interestingly, positively selected sites include several serine residues suggesting modifications in protein function and/or localization among Primates. Our results suggest that positive selection is driven by aspects related to species-specific adaptations to fertilization rather than sexual selection.

Highlights

  • Molecular evolutionary analysis of protein coding genes show that most genes evolve under purifying selection with few exceptions of rapid change between species driven by positive selection [1, 2]

  • The JTT model of sequence evolution [27] with G, the shape parameter for the gamma distribution, and F, the amino acid frequencies, was identified as the best fit for phylogenetic reconstruction of the izumo gene family according to its AIC value (JTT+G+F: lnL = −14693.74; AIC = 29641.5)

  • We have not found a consistent pattern of selection for a specific izumo gene across phylogenetic groups but rather signals that are gene and phylogenetic group specific

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Summary

Introduction

Molecular evolutionary analysis of protein coding genes show that most genes evolve under purifying selection with few exceptions of rapid change between species driven by positive selection [1, 2]. Many male reproductive genes have shown evidence of rapid evolution driven by positive selection [4,5,6]. It has been more difficult, to link positive selection to sexual selection, and numerous hypotheses have been proposed to explain this difficulty [7, 8]. Gorillas, with a polygamous mating system, have lost SEMG1 gene function entirely [14] These studies seem to suggest that sexual selection bouts have been phylogenetically restricted or perhaps “softened” for SEMG1 but not SEMG2

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