Proteins Involved in Motility and Sperm-Egg Interaction Evolve More Rapidly in Mouse Spermatozoa

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.

Characterization of a male reproductive transcriptome forPeromyscus eremicus(Cactus mouse)

“…Leucine-rich repeat containing (Lrrc) genes have diverse biological roles; therefore, we also will not speculate on any correspondence between these two genes. As expected given our experimental design, there was no concordance between our 42 genes and those found to be under positive selection in a recent study on mouse spermatozoa proteins (Vicens, Luke & Roldan, 2014). …”

“…In addition, the epididymal transcriptome of M. musculus shows evidence for positive selection among epididymis-specialized genes that are secreted, which the authors attribute to their putative evolutionary importance (Dean, Good & Nachman, 2008). Moreover, a recent analysis for sperm genes from multiple mouse strains found that sperm proteins involved in both motility and in sperm-egg interactions show signatures of positive selection, potentially facilitating evolutionary mechanisms for sperm-competition and sexual conflict (Vicens, Luke & Roldan, 2014). We therefore propose that both the inherently costly nature of producing ejaculate and the rapid evolution of genes in murine testes, epididymis, and sperm would be ideal for desert rodents to evolve ejaculate adaptations to limited water-availability.…”

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis

“…Therefore, rapid evolution of sperm genes appears to be the most reasonable 425 explanation for the breakdown of reciprocal relationships (see below). This conclusion is consistent with 426 a diverse body of evidence that supports the influence of positive selection on male reproductive genes 427 [62,65], including those functioning in sperm [43,[66][67][68]. We note that we cannot rule out the influence 428 of de novo creation but it is currently difficult to assess the contribution of this mechanism to the overall 429…”

Effects of different kinds of essentiality on sequence evolution of human testis proteins

“…16). Based on nucleotide sequences of different mouse strains and species, Vicens et al 18. found higher proportions of genes with signals of positive selection in groups linked to sperm-egg interaction and sperm motility than in four other categories.…”