Selection in the Rapid Evolution of Gamete Recognition Proteins in Marine Invertebrates

Abstract

Animal fertilization is governed by the interaction (binding) of proteins on the surfaces of sperm and egg. In many examples presented herein, fertilization proteins evolve rapidly and show the signature of positive selection (adaptive evolution). This review describes the molecular evolution of fertilization proteins in sea urchins, abalone, and oysters, animals with external fertilization that broadcast their gametes into seawater. Theories regarding the selective forces responsible for the rapid evolution driven by positive selection seen in many fertilization proteins are discussed. This strong selection acting on divergence of interacting fertilization proteins might lead to prezygotic reproductive isolation and be a significant factor in the speciation process.Since only a fraction of all eggs are fertilized and only an infinitesimal fraction of male gametes succeed in fertilizing an egg, gametes are obviously a category of entities subjected to intense selection. It is curious that this is never mentioned in the literature dealing with selection, perhaps because we know so little about fitness differences among gametes.(Ernst Mayr, 1997)

Genetic conflicts: the usual suspects and beyond

“…As sperm competition will inevitably select for 'faster binding', this divergent interest results in perpetual cycles of adaptation and counter-adaptation. Indeed, sperm and egg proteins have been shown to be among the most rapidly evolving in plant and animal genomes (Swanson and Vacquier, 2002;Vacquier and Swanson, 2011), consistent with the sperm-egg interface representing a Red Queen interaction.…”

Cryptic species diversity and reproductive isolation among sympatric lineages ofStrongylocentrotussea urchins in the northwest Atlantic

“…The rapid evolution of gamete recognition molecules has long been considered an important driver of speciation in Echinoderms (Vacquier 1998;Palumbi 2009;Lessios 2011;Vacquier and Swanson 2011). Both proteins and carbohydrates (sulfated polysaccharides) coating the sperm and eggs mediate gamete interactions in the plankton and are involved in sperm competition and mate choice (Biermann et al 2004).…”

Is Sexual Conflict an "Engine of Speciation"?

“…The data also indicate a potential role for reinforcement, because, in some cases, the rate of evolution and the extent of polymorphism correlate with the number of sympatric species (Vacquier and Swanson 2011). However, rapid evolution of fertilization proteins is not universal.…”

“…At least in the case of marine organisms, there now appears to be a consensus that these data can be explained in large part by selection for avoidance of polyspermy (Levitan et al 2007;Palumbi 2009;Lessios 2011;Vacquier and Swanson 2011). Sperm is under strong selection for increased efficiency in fertilizing eggs, but if more than one sperm penetrates the egg, the resulting zygote in usually inviable.…”

“…However, rapid evolution of fertilization proteins is not universal. For example, for some allopatric species of sea urchins that diverged more than 4-9 million years, there is no evidence of positive selection in bindin alleles that evolve very rapidly in other species (Vacquier and Swanson 2011).…”