Genetic contributions to ectopic sperm cell migration in Caenorhabditis nematodes

Abstract Reproductive barriers involving gametic incompatibilities can act to enhance population divergence and promote the persistence of species boundaries. Observing gametic interactions in internal fertilizing organisms, however, presents a considerable practical challenge to characterizing mechanisms of such gametic isolation. Here we exploit the transparency of Caenorhabditis nematodes to investigate gametic isolation mediated by sperm that can migrate to ectopic locations, with this sperm invasion capable of inducing female sterility and premature death. As a step toward identifying genetic factors and mechanisms associated with female susceptibility to sperm invasion, we characterized a panel of 25 C. elegans genetic mutants to test for effects on the incidence and severity of sperm invasion in both conspecific and interspecies matings. We found genetic perturbations to contribute to distinct patterns of susceptibility that identify ovulation dynamics and sperm guidance cues as modulators of ectopic sperm migration incidence and severity. Genotypes confer distinctive phenotypic sensitivities to the sperm from conspecific C. elegans males versus heterospecific C. nigoni males, implicating evolution of functional divergence in the history of these species for components of sperm-reproductive tract interactions. Sexually-antagonistic co-evolution within species that drives divergent trait and molecular evolution between species provides a working model to explain mismatched species-specific gametic interactions that promote or mitigate ectopic sperm migration. Article Summary Here we exploit the transparency of C. elegans roundworms to investigate reproductive barriers between species resulting from sperm-cell invasion into ectopic tissues, causing female sterility and premature death. We quantify female sensitivity to sperm invasion from conspecific and interspecific matings in a panel of 25 C. elegans genetic mutants, to demonstrate how ovulation dynamics and sperm guidance cues act as modulators of ectopic sperm-cell migration incidence and severity. We observe both conserved and divergent responses to different species, implicating evolution of functional divergence for components of sperm-reproductive tract interactions consistent with the outcome of sexually-antagonistic co-evolution.