Incipient speciation of sea star populations by adaptive gamete recognition coevolution

Reproductive isolation--the key event in speciation--can evolve when sexual conflict causes selection favoring different combinations of male and female adaptations in different populations. Likely targets of such selection include genes that encode proteins on the surfaces of sperm and eggs, but no previous study has demonstrated intraspecific coevolution of interacting gamete recognition genes under selection. Here, we show that selection drives coevolution between an egg receptor for sperm (OBi1) and a sperm acrosomal protein (bindin) in diverging populations of a sea star (Patiria miniata). We found positive selection on OBi1 in an exon encoding part of its predicted substrate-binding protein domain, the ligand for which is found in bindin. Gene flow was zero for the parts of bindin and OBi1 in which selection for high rates of amino acid substitution was detected; higher gene flow for other parts of the genome indicated selection against immigrant alleles at bindin and OBi1. Populations differed in allele frequencies at two key positively selected sites (one in each gene), and differences at those sites predicted fertilization rate variation among male-female pairs. These patterns suggest adaptively evolving loci that influence reproductive isolation between populations.