SIMULTANEOUS POSITIVE AND NEGATIVE FREQUENCY-DEPENDENT SELECTION ON SPERM BINDIN, A GAMETE RECOGNITION PROTEIN IN THE SEA URCHINSTRONGYLOCENTROTUS PURPURATUS

Abstract

Gamete-recognition proteins often, but not always, evolve rapidly. We explored how variation in sperm bindin influences reproductive success of the sea urchin Strongylocentrotus purpuratus during group spawning in the sea. Despite large variation in male and female abundance and neighbor distances, males with common genotypes had higher reproductive success than males with rare genotypes. However, males with a relatively uncommon proline-for-serine substitution were the most successful. Females also showed a fitness consequence of sperm-bindin genotype, suggesting linkage disequilibrium between the sperm-bindin locus and the egg receptor locus. Females with common genotypes had higher reproductive success than rare genotypes, but females with relatively uncommon insertions were most successful. Overall, these results suggest that rare male proteins are selected against, as supported by molecular evidence of purifying selection and probably caused by poor matches to the female receptor protein. Within the pool of moderately common to common alleles, however, individuals with less-common functional variants were favored and probably maintained by negative frequency-dependent selection. These results support the hypothesis that sperm availability and sexual conflict influence the evolution of gamete recognition systems in broadcast spawners and highlight the benefits of combining fitness measures with molecular signatures for estimation of patterns of selection.

Density drives polyandry and relatedness influences paternal success in the Pacific gooseneck barnacle, Pollicipes elegans

“…Experimental work on the sperm-bindin locus and receptor in various sea urchin species has shown that males with more common or matching bindin genotypes perform better in sperm competition, resulting in greater reproductive success (though this is also mediated by the density of conspecifics and availability of sperm: (e.g. [35,67]). Alternatively, a number of studies show that differential embryo survival influences paternity bias, and its inference [68-70].…”

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

“…However, in the north Atlantic, S. droebachiensis is the only species of sea urchin in the shallow subtidal (<30 m) where population densities can reach 400 m −2 (Scheibling and Hennigar 1997). High sperm density in these populations can result in high variance in reproductive success caused by polyspermy (Levitan 2004(Levitan , 2005, leading to sexual conflict as males are selected for fast fertilization and females are selected to prevent polyspermy by reducing fertilization rates (Levitan 2004;Levitan and Ferrell 2006;Levitan et al 2007;Levitan and Stapper 2010). Under this scenario, the eggs of S. droebachiensis in northwest Atlantic populations may have co-evolved mechanisms that indirectly reduce the susceptibility to heterospecific sperm and thus prevent hybridization.…”

Rates of sea urchin bindin evolution

“…Eggs are fertilized at higher rates by sperm carrying the same bindin allele. Using the same proxy, Levitan and Farrell (2006) and Levitan and Stapper (2010) showed in Strongylocentrotus franciscanus and S. purpuratus that sperm density and the danger of polyspermy establish different selective regimes for various bindin alleles. At low sperm densities, most offspring are produced by the union of sperm and egg possessing bindin alleles that are most common in the population.…”