Sexual Selection and the Adaptive Evolution of Mammalian Ejaculate Proteins

Abstract

An elevated rate of substitution characterizes the molecular evolution of reproductive proteins from a wide range of taxa. Although the selective pressures explaining this rapid evolution are yet to be resolved, recent evidence implicates sexual selection as a potentially important explanatory factor. To investigate this hypothesis, we sought evidence of a high rate of adaptive gene evolution linked to postcopulatory sexual selection in muroid rodents, a model vertebrate group displaying a broad range of mating systems. Specifically, we sequenced 7 genes from diverse rodents that are expressed in the testes, prostate, or seminal vesicles, products of which have the potential to act in sperm competition. We inferred positive Darwinian selection in these genes by estimation of the ratio of nonsynonymous (d(N), amino acid changing) to synonymous (d(S), amino acid retaining) substitution rates (omega = d(N)/d(S)). Next, we tested whether variation in this ratio among lineages could be attributed to interspecific variation in mating systems, as inferred from the variation in these rodents' relative testis sizes (RTS). Four of the 7 genes examined (Prm1, Sva, Acrv1, and Svs2, but not Svp2, Msmb, or Spink3) exhibit unambiguous evidence of positive selection. One of these, the seminal vesicle-derived protein Svs2, also shows some evidence for a concentration of positive selection in those lineages in which sperm competition is common. However, this was not a general trend among all the rodent genes we examined. Using the same methods, we then reanalyzed previously published data on 2 primate genes, SEMG1 and SEMG2. Although SEMG2 also shows evidence of positive selection concentrated in lineages subject to high levels of sperm competition, no such trend was found for SEMG1. Overall, despite a high rate of positive selection being a feature of many ejaculate proteins, these results indicate that the action of sexual selection potentially responsible for elevated evolutionary rates may be difficult to detect on a gene-by-gene basis. Although the extreme diversity of reproductive phenotypes exhibited in nature attests to the power of sexual selection, the extent to which this force predominates in driving the rapid molecular evolution of reproductive genes therefore remains to be determined.

Genetic and phenotypic influences on copulatory plug survival in mice

“…Consistent with a hypothesis of sexual conflict (Stockley, 1997), recently mated females upregulate proteases thought to assist in plug degradation (Kelleher and Pennington, 2009;Dean et al, 2011), whereas male seminal fluid is enriched for protease inhibitors , although proteases and their inhibitors have additional roles in reproduction (Wolfner, 2002;Kawano et al, 2010). Also, plug-forming proteins, proteases and protease inhibitors all tend to evolve rapidly (Dorus et al, 2004;Clark and Swanson, 2005;Kelleher et al, 2007;Lawniczak and Begun, 2007;Ramm et al, 2008;Wong et al, 2008;Dean and Nachman, 2009;Dean et al, 2011) as predicted for genes involved in sexual conflict (Swanson and Vacquier, 2002;Clark et al, 2006). In primates, the evolutionary rate of a key copulatory plug gene, SEMG2, is positively correlated with the inferred intensity of sexual selection (Dorus et al, 2004;Ramm et al, 2009).…”

Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal

“…This new finding highlights the importance of non-sperm ejaculate components in rodent sperm competition (see also [48,49]) and the significance of sperm competition-induced phenotypic plasticity for explaining intraspecific variation in vertebrate reproductive traits [29,54].…”

“…Recent studies highlight the likely functional significance of such plugs in mammalian sperm competition. For example, comparative studies of rodents reveal that higher levels of sperm competition are associated with relatively large seminal vesicles and mating plugs [14], a faster rate of molecular evolution among seminal vesicle-expressed genes [48], and a higher molecular mass of SVS II, a key protein involved in plug formation [49]. Although the precise function of mammalian copulatory plugs is uncertain, roles in promoting sperm transport and/or reducing the rate of female remating in the context of sperm competition appear likely [14,47].…”

Proteomics enhances evolutionary and functional analysis of reproductive proteins

“…In rodents, the evolutionary rate of SVS II, a protein that becomes cross-linked upon insemination to form the copulatory plug, is correlated with testis size, a proxy for the level of sperm competition. (37,78) These studies suggest that in mammals, the mating system is an important factor that influences the rate of reproductive protein evolution. In Drosophila, more promiscuous species may have more rapidly evolving reproductive proteins, (79) and with the new availability of larger data sets for male (34) and female (17) proteins of these species, we expect progress in identifying those proteins whose evolutionary histories have been most affected by mating system changes.…”