Sexual selection on protamine and transition nuclear protein expression in mouse species

Abstract

Post-copulatory sexual selection in the form of sperm competition is known to influence the evolution of male reproductive proteins in mammals. The relationship between sperm competition and regulatory evolution, however, remains to be explored. Protamines and transition nuclear proteins are involved in the condensation of sperm chromatin and are expected to affect the shape of the sperm head. A hydrodynamically efficient head allows for fast swimming velocity and, therefore, more competitive sperm. Previous comparative studies in rodents have documented a significant association between the level of sperm competition (as measured by relative testes mass) and DNA sequence evolution in both the coding and promoter sequences of protamine 2. Here, we investigate the influence of sexual selection on protamine and transition nuclear protein mRNA expression in the testes of eight mouse species that differ widely in levels of sperm competition. We also examined the relationship between relative gene expression levels and sperm head shape, assessed using geometric morphometrics. We found that species with higher levels of sperm competition express less protamine 2 in relation to protamine 1 and transition nuclear proteins. Moreover, there was a significant association between relative protamine 2 expression and sperm head shape. Reduction in the relative abundance of protamine 2 may increase the competitive ability of sperm in mice, possibly by affecting sperm head shape. Changes in gene regulatory sequences thus seem to be the basis of the evolutionary response to sexual selection in these proteins.

Intra-Protein Coevolution Is Increasingly Functional with Greater Proximity to Fertilization

“…In fact, it seems reasonable to assume that natural selection prevails in the body-wide proteome, and the same should be true for the liver proteome [e.g., Bersaglieri et al, 2004;Qiu et al, 2008;Blekhman et al, 2014]. Compared to this, the impact of postcopulatory forms of sexual selection should increase with greater closeness to fertilization [Gasparini and Pilastro, 2011;Løvlie et al, 2013;Lüke et al, 2014;Ramm et al, 2014;Sirot et al, 2014;Zhou et al, 2015]. At the molecular level, present results would be in accordance with a growing proportion of outward coevolution with greater proximity to fertilization.…”

“…Numerous male reproductive proteins show elevated rates of sequence evolution [e.g., Torgerson et al, 2002;Clark and Swanson, 2005;Haerty et al, 2007]. The probable driving force behind is commonly seen in the various forms of postcopulatory sexual selection, including sperm competition [e.g., Lüke et al, 2014;Ramm et al, 2014;Schumacher et al, 2014], cryptic female choice [Gasparini and Pilastro, 2011;Løvlie et al, 2013], and sexual conflict Sirot et al, 2014]. Prominent examples of male reproductive genes under postcopulatory sexual selection are primate and rodent protamines and semenogelins, whereby the first replace histones in the sperm head [Wyckoff et al, 2000;Ramm et al, 2008;Lüke et al, 2014] and the latter polymerize to a copulation plug in the female genital tract [Jensen-Seaman and Li, 2003;Dorus et al, 2004;Ramm et al, 2008].…”

“…The probable driving force behind is commonly seen in the various forms of postcopulatory sexual selection, including sperm competition [e.g., Lüke et al, 2014;Ramm et al, 2014;Schumacher et al, 2014], cryptic female choice [Gasparini and Pilastro, 2011;Løvlie et al, 2013], and sexual conflict Sirot et al, 2014]. Prominent examples of male reproductive genes under postcopulatory sexual selection are primate and rodent protamines and semenogelins, whereby the first replace histones in the sperm head [Wyckoff et al, 2000;Ramm et al, 2008;Lüke et al, 2014] and the latter polymerize to a copulation plug in the female genital tract [Jensen-Seaman and Li, 2003;Dorus et al, 2004;Ramm et al, 2008]. Also, vertebrate sperm proteins like zonadhesin that bind to the zona pellucida or the oocyte are known for elevated rates of sequence divergence [Swanson et al, 2003;Herlyn and Zischler, 2006;Dorus et al, 2010;Claw et al, 2014].…”

Re-visiting the Protamine-2 locus: deletion, but not haploinsufficiency, renders male mice infertile

“…This is suggestive for a PRM1/2 coregulation in order to maintain the mouse specific PRM1/2 ratio. Recent analyses revealed that PRM1/PRM2 ratio range from 65% ( M. castaneus and M. domesticus ) to 99% ( M. macedonicus and M. spicilegus ) in different mouse subspecies56. This indicates that mice might be able to tolerate changes in the PRM1/2 ratio to some extent.…”

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

“…changes in protamination or compaction) appear not be in place in these species to counteract the damaging effects of ROS on sperm DNA. However, differences in the type and extent of protamination in relation to levels of sperm competition deserve future examination [50].…”