Abstract
Proteomic studies of spermatozoa have identified a large catalog of integral sperm proteins. Rapid evolution of these proteins may underlie adaptive changes of sperm traits involved in different events leading to fertilization, although the selective forces underlying such rapid evolution are not well understood. A variety of selective forces may differentially affect several steps ending in fertilization, thus resulting in a compartmentalized adaptation of sperm proteins. Here we analyzed the evolution of genes associated to various events in the sperm’s life, from sperm formation to sperm-egg interaction. Evolutionary analyses were performed on gene sequences from 17 mouse strains whose genomes have been sequenced. Four of these are derived from wild Mus musculus, M. domesticus, M. castaneus and M. spretus. We found a higher proportion of genes exhibiting a signature of positive selection among those related to sperm motility and sperm-egg interaction. Furthermore, sperm proteins involved in sperm-egg interaction exhibited accelerated evolution in comparison to those involved in other events. Thus, we identified a large set of candidate proteins for future comparative analyses of genotype-phenotype associations in spermatozoa of species subjected to different sexual selection pressures. Adaptive evolution of proteins involved in motility could be driven by sperm competition, since this selective force is known to increase the proportion of motile sperm and their swimming velocity. On the other hand, sperm proteins involved in gamete interaction could be coevolving with their egg partners through episodes of sexual selection or sexual conflict resulting in species-specific sperm-egg interactions and barriers preventing interspecies fertilization.
Highlights
Sexual reproduction is a fundamental biological process common among eukaryotes
Distribution of Sperm Proteins A dataset of 1,350 proteins was gathered based on evidence of their presence in mouse spermatozoa (Table S1)
Evolutionary Rate of Sperm Genes Nucleotide sequences of genes coding for the 165 selected sperm proteins were obtained from the genomes of 17 mouse strains and species (Fig. 1)
Summary
Sexual reproduction is a fundamental biological process common among eukaryotes. At the molecular level, reproduction is an intricate process that involves interactions between many proteins. Numerous studies have shown a rapid evolution of these so-called reproductive proteins and, the idea that genes involved in reproductive processes evolve rapidly has gained widespread acceptance [1,2,3,4]. Rates of molecular evolution may vary depending on the different steps of the reproductive process, timing of gene expression, and the tissue or organ in which genes are expressed [7,8,9]. Heterogeneity in evolutionary rates has even been found in the mature sperm proteome and, most sperm proteins seem to be under functional constraints and only a small subset appears to evolve rapidly [10]. Controversial hypotheses exist regarding proteins with testis-specific expression that evolve more rapidly than proteins with expression in other tissues [10,11]
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