Sexual selection and the adaptive evolution of PKDREJ protein in primates and rodents

Abstract

PKDREJ is a testis-specific protein thought to be located on the sperm surface. Functional studies in the mouse revealed that loss of PKDREJ has effects on sperm transport and the ability to undergo an induced acrosome reaction. Thus, PKDREJ has been considered a potential target of post-copulatory sexual selection in the form of sperm competition. Proteins involved in reproductive processes often show accelerated evolution. In many cases, this rapid divergence is promoted by positive selection which may be driven, at least in part, by post-copulatory sexual selection. We analysed the evolution of the PKDREJ protein in primates and rodents and assessed whether PKDREJ divergence is associated with testes mass relative to body mass, which is a reliable proxy of sperm competition levels. Evidence of an association between the evolutionary rate of the PKDREJ gene and testes mass relative to body mass was not found in primates. Among rodents, evidence of positive selection was detected in the Pkdrej gene in the family Cricetidae but not in Muridae. We then assessed whether Pkdrej divergence is associated with episodes of sperm competition in these families. We detected a positive significant correlation between the evolutionary rates of Pkdrej and testes mass relative to body mass in cricetids. These findings constitute the first evidence of post-copulatory sexual selection influencing the evolution of a protein that participates in the mechanisms regulating sperm transport and the acrosome reaction, strongly suggesting that positive selection may act on these fertilization steps, leading to advantages in situations of sperm competition.

Parallel Evolution of Sperm Hyper-Activation Ca2+ Channels

“…Interestingly, these are not the first polycystic kidney disease domain containing genes that have been shown to evolve rapidly in the context of reproductive functions. PKDREJ is a sperm receptor for egg-coat proteins which controls the timing of the acrosome reaction ( Sutton et al 2008 ), and it has evolved rapidly under positive selection across primates and murine species ( Hamm et al 2007 ; Vicens et al 2015 ). PKDREJ may act as an ion channel via its PKD domain, though its molecular function is not well characterized.…”

“…These rapid changes in reproductive proteins have the potential to establish barriers to fertilization between populations and lead to the evolution of new species ( Parker and Partridge 1998 ; Gavrilets 2000 ; Howard et al 2009 ; Moyle et al 2014 ). The best-known examples of this phenomenon include the rapid evolution of reproductive proteins in abalone, mammals, and Drosophila ( Lee et al 1995 ; Swanson and Vacquier 1997 ; Kresge et al 2001 ; Swanson et al 2003 ; Gomendio et al 2006 ; Clark et al 2007 ; Hamm et al 2007 ; Findlay et al 2014 ; Vicens et al 2015 ). Molecular evolutionary studies on how sexual conflicts shape reproductive proteins have focused on several aspects of sperm biology such as direct sperm-egg interactions, seminal fluid proteins and sperm behavior ( Swanson and Vacquier 2002 ; Panhuis et al 2006 ; Fisher et al 2016 ).…”

Cell Type-Specific Expression of Testis Elevated Genes Based on Transcriptomics and Antibody-Based Proteomics

“…Interestingly, 9 two MPs exclusively expressed in premeiotic germ cells with similar expression patterns are the 10 polycystic kidney disease and receptor for egg jelly-related protein (PKDREJ) and the 11 uncharacterized protein C3orf22 (C3orf22) ( Figure 3). PKDREJ has been suggested to be 12 involved in sperm transport and acrosome reaction in both rodents and primates 26 (Figure 4). This family 25 of RNA-binding proteins was isolated from the AZF region on the human Y chromosome, and is 26 frequently deleted in infertile men with non-obstructive azoospermia [29][30] .…”

“…TIPIN has never been 18 described in the testis, however, its known function in other tissues and increasing levels of 19 expression from spermatogonia to preleptotene spermatocytes in the human testis, strongly 20 suggest that TIPIN could be a key player in the regulation of DNA replication during the premeiotic 21 S phase in spermatogenesis.22 23Another interesting protein expressed in spermatogonia and preleptotene spermatocytes is the 24 sarcoma antigen 1 (SAGE1) protein, also named cancer/testis antigen 14 (Figure 3). Like most 25 cancer/testis antigens (CTAs), SAGE1 expression in normal tissues is restricted to the testis,26 while strong expression is observed in several carcinomas 25 . SAGE1 is a PE1 protein supposedly…”

Parallel evolution of sperm hyper-activation Ca2+channels

“…These rapid changes in reproductive proteins have the potential to establish barriers to fertilization between populations and lead to the evolution of new species (Parker and Partridge 1998;Gavrilets 2000;Howard et al 2009;Moyle et al 2014). The best-known examples of this phenomenon include the rapid evolution of reproductive proteins in abalone, mammals, and Drosophila (Lee et al 1995;Swanson and Vacquier 1997;Kresge et al 2001;Swanson et al 2003;Clark et al 2007;Hamm et al 2007;Findlay et al 2014;Vicens et al 2015). Molecular evolutionary studies on how sexual conflicts shape reproductive proteins have focused on several aspects of sperm biology such as direct sperm-egg interactions, seminal fluid proteins and sperm behavior (Swanson and Vacquier 2002;Panhuis et al 2006;Fisher et al 2016).…”