Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity

Abstract

Postcopulatory sperm competition is a key aspect of sexual selection and is believed to drive the rapid evolution of both reproductive physiology and reproduction-related genes. It is well-established that mating behavior determines the intensity of sperm competition, with polyandry (i.e., female promiscuity) leading to fiercer sperm competition than monandry. Studies in mammals, particularly primates, showed that, owing to greater sperm competition, polyandrous taxa generally have physiological traits that make them better adapted for fertilization than monandrous species, including bigger testes, larger seminal vesicles, higher sperm counts, richer mitochondrial loading in sperm and more prominent semen coagulation. Here, we show that the degree of polyandry can also impact the dynamics of molecular evolution. Specifically, we show that the evolution of SEMG2, the gene encoding semenogelin II, a main structural component of semen coagulum, is accelerated in polyandrous primates relative to monandrous primates. Our study showcases the intimate relationship between sexual selection and the molecular evolution of reproductive genes.

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).…”

“…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).…”

The androgen receptor and prostate cancer: A role for sexual selection and sexual conflict?

“…A number of seminal proteins in Drosophila, such as the accessory gland protein Acp26Aa, have been shown to exhibit rapid evolution and high ratios of non-synonymous to synonymous substitution, a hallmark of positive selection [10]. In mammals in general [11] and primates in particular [12], seminal proteins have been found to evolve rapidly and show evidence of positive selection related to sexual selection and sexual conflict. Sexual selection and sexual conflict are thus expected to act on the proteins that make up this locus of interaction.…”

The semenogelins: proteins with functions beyond reproduction?

“…Naturally, as major constituents of semen, the semenogelins are closely associated with reproduction, and a large proportion of our knowledge on these proteins consists of results and hypotheses related to fertility [16]. A correlation has been found between the degree of female promiscuity within a species and the evolution of the two genes encoding 3 semenogelins I and II, and thus it has been suggested that post-copulatory sperm competition drives the evolution of these genes [13,17,18]. In addition to having coagulum-forming functions and being susceptible to cleavage by kallikrein-like peptidases, the semenogelins are assumed to activate sperm hyaluronidase [19], affect sperm motility [20], possess antimicrobial activity [21], serve as substrates for transglutaminase [22], and have amyloid properties [23].…”