Evolution of gamete compatibility and reproductive isolation

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Coevolving gene pairs mediate interactions between gametes or between mates, and may be subject to intense sexual selection (sperm competition, reproductive conflicts of interest). This coevolution is of interest to evolutionary biologists because selection on genetic differences among individuals can lead to genetic and reproductive differences between populations and species. The same processes are also of interest to ecologists and physicians because the coevolution of the maternal and paternal genomes can produce coadapted gene pairs with high fertility as well as mismatched pairs with lower fertility. I propose four related studies of reproductive compatibility evolving on different time scales from contemporary within-population differences (in sea stars and humans) to between-species differences (in sister species of sea stars and nudibranchs). We showed that selection on two gamete-binding genes (bindin, OBi1) from two deeply diverging (>70,000 years) populations of the bat star (Patiria miniata) strongly influences sperm-egg compatibility. I now propose to carry out a conceptual replication of that study to test the effects of paternal-maternal mismatches on fertilization rates between mates from the same single population of P. miniata. Such replication studies are rare in evolutionary ecology. We discovered selection and coevolution among three gamete-binding genes (C4BPA, ZP2, ZP3) from human population groups. I now propose to analyze these coevolving pairs of genes in human couples seeking treatment for infertility in western Canada. We ask how maternal-paternal mismatches might account for specific forms of infertility that are amenable to different clinical treatment options. We discovered very recent divergence (<10,000 years) between sister species of sea stars from tropical eastern Australia, including one species with the typical sea star mating system (Cryptasterina pentagona with separate sexes, planktonic fertilization by outcrossing) and one with a highly derived mating system (C. hystera with hermaphrodites, internal self-fertilization, live birth of juveniles). We will take advantage of the impending development of a high-quality Cryptasterina reference genome to assemble and compare multiple genomes from both species, and to find and characterize the genomic regions associated with species differences in sex and reproduction. Our new collaborators in the USA and Canada recently discovered that the charismatic nudibranch Hermissenda crassicornis, which is a model organism in neuroscience, is a complex of three closely related and phenotypically similar species, including H. crassicornis s.s. & H. opalescens from the Pacific coast of North America. Our collaborators shared genomic sequence data for both those species, and we will analyze those data (and collect new data) to discover the demographic history of the speciation event (especially the age of the speciation event, and gene flow between the two species).