Abstract
BackgroundGenes that encode proteins associated with sperm competition, fertilization, and sexual conflicts of interest are often among the most rapidly evolving parts of animal genomes. One family of sperm-expressed genes (Zp3r, C4bpa) in the mammalian gene cluster called the regulator of complement activation (RCA) encodes proteins that bind eggs and mediate reproductive success, and are therefore expected to show high relative rates of nonsynonymous nucleotide substitution in response to sexual selection in comparison to other genes not involved in gamete binding at fertilization. We tested that working hypothesis by using phylogenetic models of codon evolution to identify episodes of diversifying positive selection. We used a comparative approach to quantify the evidence for episodic diversifying selection acting on RCA genes with known functions in fertilization (and sensitivity to sexual selection), and contrast them with other RCA genes in the same gene family that function in innate immunity (and are not sensitive to sexual selection).ResultsWe expected but did not find evidence for more episodes of positive selection on Zp3r in Glires (the rodents and lagomorphs) or on C4BPA in Primates, in comparison to other paralogous RCA genes in the same taxon, or in comparison to the same orthologous RCA gene in the other taxon. That result was not unique to RCA genes: we also found little evidence for more episodes of diversifying selection on genes that encode selective sperm-binding molecules in the egg coat or zona pellucida (Zp2, Zp3) in comparison to members of the same gene family that encode structural elements of the egg coat (Zp1, Zp4). Similarly, we found little evidence for episodic diversifying selection acting on two other recently discovered genes (Juno, Izumo1) that encode essential molecules for sperm–egg fusion.ConclusionsThese negative results help to illustrate the importance of a comparative context for this type of codon model analysis. The results may also point to other phylogenetic contexts in which the effects of selection acting on these fertilization proteins might be more readily discovered and documented in mammals and other taxa.
Highlights
Genes that encode proteins associated with sperm competition, fertilization, and sexual conflicts of interest are often among the most rapidly evolving parts of animal genomes
Episodic diversifying selection on regulator of complement activation (RCA) genes Zona pellucida 3 receptor (Zp3r), Alpha subunit of C4b-binding protein (C4bpa) and Beta subunit of C4b-binding protein (C4bpb) We used the adaptive branch-site random effects likelihood model to identify episodes of selection associated with specific lineages, and to test the hypothesis of more episodes of positive selection in genes that encode proteins involved in gamete binding or fusion
We found 11 episodes of selection acting on the two RCA genes expressed in sperm, including three episodes of positive selection on Zp3r in the deer mouse and both species of Castorimorpha, and four episodes of positive selection on C4BPA in the bush baby, tarsier, and two Old World monkeys (Table 1; Fig. 2)
Summary
Genes that encode proteins associated with sperm competition, fertilization, and sexual conflicts of interest are often among the most rapidly evolving parts of animal genomes. Genes that encode molecules expressed on the surfaces of gametes are key to the success of several interactions among males or between males and females, including sperm chemoattraction toward the egg, gamete physiological activation (including the sperm acrosome reaction), sperm binding to the egg coat, and fusion of gametes [26, 52] Such genes are among the most rapidly evolving parts of animal genomes [34, 80], in part. Several studies have documented high rates of molecular evolution of Zp2 and Zp3 among closely related mammal species, including episodes of diversifying or positive selection on codons in the known sperm-binding domains of rodent genes [66, 67, 69, 72, 73], and population genetic analyses indicate selection on ZP2 and ZP3 in humans ([24, 58]; for counterexamples see [2, 13, 41])
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