Genetic contributions to ectopic sperm cell migration inCaenorhabditisnematodes

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 spermreproductive 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 SummaryHere 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.

Reproductive transitions in plants and animals: selfing syndrome, sexual selection and speciation

“…For example, excessively rapid pollen tube growth in unripe pistils leads to low seed set in Collinsia (Madjidian et al ., ). This aggressive pollen phenomenon is analogous to sexually antagonistic aggressive sperm in Caenorhabditis nematodes that invade gonad tissues and reduce female fitness (Ting et al ., , ).…”

Natural Variation and Genetic Determinants of Caenorhabditis elegans Sperm Size

“…While the size of amoeboid Caenorhabditis sperm can be a critical factor for sperm competitive ability, recent work has uncovered crucial roles of genetic factors in Caenorhabditis sperm competition that act independently of sperm size (Thomas et al 2012;Ting et al 2014Ting et al , 2018Fierst et al 2015;Hansen et al 2015;Yin et al 2018;Yin and Haag 2019). Most prominently, genome shrinkage observed in the three androdioecious Caenorhabditis species involves a strong bias in the loss of male-expressed genes, including the parallel loss of the male secreted short (mss) gene family, which is critical for sperm competitive ability in gonochoristic species (Thomas et al 2012;Fierst et al 2015;Yin et al 2018).…”

Measuring Sperm Guidance and Motility within the <em>Caenorhabditis elegans</em> Hermaphrodite Reproductive Tract

“…The molecular mechanisms by which spermatozoa (referred to as sperm) navigate through the female reproductive tract toward the oocyte are not well understood, yet are fundamental to sexual reproduction. Sperm motility is highly dynamic and depends on robust communication signals that alter sperm velocity and directional motility 1,2,3,4,5,6,7,8,9,10,11,12 . C. elegans has become a powerful model for studying sperm movement in vivo because the hermaphrodite's transparent epidermis permits the tracking of live sperm at single cell resolution 2,3,8,10 .…”

“…Sperm motility is highly dynamic and depends on robust communication signals that alter sperm velocity and directional motility 1,2,3,4,5,6,7,8,9,10,11,12 . C. elegans has become a powerful model for studying sperm movement in vivo because the hermaphrodite's transparent epidermis permits the tracking of live sperm at single cell resolution 2,3,8,10 . The purpose of this paper is to provide methods for assessing sperm movement within the C. elegans hermaphrodite uterus.…”

“…Molecules can be injected into the hermaphrodite gonad to test for effects on sperm activation, migration velocity, and directional motility 3 . Additionally, the described methods can be used to monitor rogue sperm migration into ectopic body locations and to evaluate sperm competition 10,14 .…”