Structure, Function, & Evolution of a Novel Sperm Competition Protein

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Shifts in reproductive mode are among the most striking events in the recent evolutionary history of animals and plants. In Caenorhabditis round worms (nematodes), self-fertile hermaphrodites have repeatedly evolved from female ancestors by acquiring the ability to make sperm in an otherwise female ovary. This developmental novelty radically alters how genes flow through populations, and greatly reduces male-male competition, with many potential downstream consequences. This project is motivated by the observations that self-fertile species have lost thousands of genes (many with roles in male reproduction), and that ancestral reproductive traits are degraded. It examines the male secreted short (mss) gene family, which appear to connect these two phenomena. MSS proteins are small, cell surface factors with an ancient role in mediating competition between sperm of different males, and were consistently lost when selfing evolved. This research serves as a case study for two relatively common phenomena in evolution. One is simplification and loss of ancestral traits. As the research unfolds, the PI will partner with informal science education professionals to bring this often counter-intuitive process to the public in two different forums. The other is the rapid evolution of genes that function in reproduction. As the sperm of both parasitic nematodes and of humans have analogous, fast-evolving proteins on their surface, the research may have eventual implications for medicine, agriculture, and human fertility. Undergraduates from groups underrepresented in science will be involved in the research and educational goals of the project. The PI and his colleagues hypothesize that relaxed selection, and possibly selection for a hermaphrodite-biased ratio, promote the loss of formerly important reproduction-related genes in self-fertile species. They also hypothesize that the MSS glycoproteins function via interactions between their post-translational carbohydrate modifications and female tissues. Four aims together will clarify the structure, function, and evolution of this intriguing family:Aim 1. Characterize the structure-function relationships of MSS proteins. Post-translational modifications of MSS proteins will be characterized, and both natural alleles and mutated transgenes will be used to infer the features of MSS proteins that are essential for their function. Aim 2. Investigate the role of MSS in sperm-sperm and sperm-female interactions. Genetics, vital dyes, and live imaging will be used to clarify how MSS proteins influence sperm competition. Attempts will also be made to identify female tissues and molecular factors that may interact with MSS. Aim 3. Characterize reproductive roles of MSS-related proteins (MSRPs) in selfing species. MSRPs are structurally similar proteins to MSS, but are found in all Caenorhabditis, regardless of mating system. MSRPs will be deleted from selfing species (which naturally already lack MSS) to determine whether they are necessary for normal fertility. Aim 4. Characterize how mss fitness interacts with mating system. We will test the hypothesis that loss of mss genes in selfing species is driven by selection for rapid population growth through experimental microcosms employing mss+ and mss- C. briggsae.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.