Simultaneous positive and negative frequency-dependent selection on sperm bindin, a gamete recognition protein in the sea urchin Strongylocentrotus purpuratus.

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.