Species whose reproductive strategies evolved at one density regime might be poorly adapted to other regimes. Field and laboratory experiments on the sea urchin Strongylocentrotus franciscanus examined the influences of the two most common sperm bindin alleles, which differ at two amino acid sites, on fertilization success. In the field experiment, the Arginine/Glycine (RG) genotype performed best at low densities and the Glycine/Arginine (GR) genotype at high densities. In the lab experiment, the RG genotype had a higher affinity with available eggs, whereas the GR genotype was less likely to induce polyspermy. These sea urchins can reach 200 years of age. The RG allele dominates in old sea urchins, whereas younger sea urchins have near equal RG and GR allele frequencies. A latitudinal cline in RG and GR genotypes is consistent with longer survival of sea urchins in the north and with predominance of RG genotypes in older individuals. The oldest sea urchins were likely conceived at low densities, before sea-urchin predators, like sea otters, were overharvested and sea urchin densities exploded off the west coast. Contemporary evolution of gamete-recognition proteins might allow species to adapt to shifts in abundances and reduces the risk of reproductive failure in altered populations.