Reproductive protein evolution within and between species: maintenance of divergent ZP3 alleles in Peromyscus

Abstract

In a variety of animal taxa, proteins involved in reproduction evolve more rapidly than nonreproductive proteins. Most studies of reproductive protein evolution, however, focus on divergence between species, and little is known about differentiation among populations within a species. Here we investigate the molecular population genetics of the protein ZP3 within two Peromyscus species. ZP3 is an egg coat protein involved in primary binding of egg and sperm and is essential for fertilization. We find that amino acid polymorphism in the sperm-combining region of ZP3 is high relative to silent polymorphism in both species of Peromyscus. In addition, while there is geographical structure at a mitochondrial gene (Cytb), a nuclear gene (Lcat) and eight microsatellite loci, we find no evidence for geographical structure at Zp3 in Peromyscus truei. These patterns are consistent with the maintenance of ZP3 alleles by balancing selection, possibly due to sexual conflict or pathogen resistance. However, we do not find evidence that reinforcement promotes ZP3 diversification; allelic variation in P. truei is similar among populations, including populations allopatric and sympatric with sibling species. In fact, most alleles are present in all populations sampled across P. truei's range. While additional data are needed to identify the precise evolutionary forces responsible for sequence variation in ZP3, our results suggest that in Peromyscus, selection to maintain divergent alleles within species contributes to the pattern of rapid amino acid substitution observed among species.

Some assembly required: evolutionary and systems perspectives on the mammalian reproductive system

“…In humans, ZP3 is a major constituent: this glycoprotein has receptor activity for sperm binding and has been shown to be under positive selection (Bleil and Wassarman 1980;Swanson et al 2001). In two Peromyscus species of mice, Hoeksta (2006, 2008b) have also found evidence for positive selection on the ZP3 gene during genus diversification and have further demonstrated that the divergent ZP3 alleles are maintained by natural selection (Turner and Hoekstra, 2006;Turner and Hoekstra, 2008b).…”

Duplication, Selection and Gene Conversion in aDrosophila mojavensisFemale Reproductive Protein Family

“…This strategy has long been hypothesized to explain the complex evolutionary histories of vertebrate MHC alleles, and their role in immune response, although the empirical data remain controversial (reviewed in Martinsohn et al 1999;Nei and Rooney 2005). Interestingly, several single-copy reproductive proteins exhibit a similar pattern of elevated polymorphism within populations, but exhibit rapid, adaptive evolution between species (Swanson et al 2001;Galindo et al 2003; Hoekstra 2006Hoekstra , 2008Gasper and Swanson 2006;Hamm et al 2007;Moy et al 2008).…”

Developmental sperm contributions: fertilization and beyond

“…There has been recent progress in functionally characterizing two promising candidate proteins that interact with ZP3: zonadhesin and PKDREJ; further, evolutionary analysis of both proteins within and between species of primates has identified promising regions of the proteins that may interact and coevolve with ZP3 (14)(15)(16).…”