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Sperm competition is found across multicellular organisms using both external and internal fertilization. Sperm competition and post-copulatory cryptic female choice can promote incompatibility between species due to antagonistic co-evolution of the sexes within a species. This between-species incompatibility is accelerated and markedly asymmetrical when sexual mode differs, producing the “weak inbreeder, strong outcrosser” (WISO) pattern. Here, we show that male secreted short (MSS) sperm glycoproteins of nematodes constitute a gametic effector of WISO. In obligately outcrossing Caenorhabditis, MSS is dispensable for baseline fertility but required for intraspecific sperm competitiveness. MSS is lost in self-fertile lineages, likely as a response to selection for a hermaphrodite-biased sex ratio. Selfing hermaphrodites that mate with males of closely related outcrossing species are rapidly sterilized due to ovarian sperm invasion. The simplification of the male proteome in selfing species suggests many factors could contribute to invasivity. However, restoration of just MSS to the self-fertile C. briggsae is sufficient to induce mild invasivity. Further, MSS+ sperm appear to derive their competitive advantage from this behavior, directly linking interspecies incompatibility with intraspecific competition. MSS-related proteins (MSRPs) remaining in the C. briggsae genome are similar in structure, expression, and localization to MSS, but are not necessary for normal sperm competitiveness. Further, over-expression of the MSRP most similar to MSS, Cbr-MSRP-3, is insufficient to enhance competitiveness. We conclude that outcrossing species retain sperm competition factors that contribute to their reproductive isolation from selfing relatives that lost them. 

Abstract Sexual characteristics and reproductive systems are dynamic traits in many taxa, but the developmental modifications that allow change and innovation are largely unknown. A leading model for this process is the evolution of self-fertile hermaphrodites from male/female ancestors. However, these studies require direct analysis of sex determination in male/female species, as well as in the hermaphroditic species that are related to them. In Caenorhabditis nematodes, this has only become possible recently, with the discovery of new species. Here, we use gene editing to characterize major sex determination genes in Caenorhabditis nigoni, a sister to the widely studied hermaphroditic species Caenorhabditis briggsae. These 2 species are close enough to mate and form partially fertile hybrids. First, we find that tra-1 functions as the master regulator of sex in C. nigoni, in both the soma and the germ line. Surprisingly, these mutants make only sperm, in contrast to tra-1 mutants in related hermaphroditic species. Moreover, the XX mutants display a unique defect in somatic gonad development that is not seen elsewhere in the genus. Second, the fem-3 gene acts upstream of tra-1 in C. nigoni, and the mutants are females, unlike in the sister species C. briggsae, where they develop as hermaphrodites. This result points to a divergence in the role of fem-3 in the germ line of these species. Third, tra-2 encodes a transmembrane receptor that acts upstream of fem-3 in C. nigoni. Outside of the germ line, tra-2 mutations in all species cause a similar pattern of partial masculinization. However, heterozygosity for tra-2 does not alter germ cell fates in C. nigoni, as it can in sensitized backgrounds of 2 hermaphroditic species of Caenorhabditis. Finally, the epistatic relationships point to a simple, linear germline pathway in which tra-2 regulates fem-3 which regulates tra-1, unlike the more complex relationships seen in hermaphrodite germ cell development. Taking these results together, the regulation of sex determination is more robust and streamlined in the male/female species C. nigoni than in related species that make self-fertile hermaphrodites, a conclusion supported by studies of interspecies hybrids using sex determination mutations. Thus, we infer that the origin of self-fertility not only required mutations that activated the spermatogenesis program in XX germ lines, but prior to these there must have been mutations that decanalized the sex determination process, allowing for subsequent changes to germ cell fates. 

Parker, Baker, and Smith provided the first robust theory explaining why anisogamy evolves in parallel in multicellular organisms. Anisogamy sets the stage for the emergence of separate sexes, and for another phenomenon with which Parker is associated: sperm competition. In outcrossing taxa with separate sexes, Fisher proposed that the sex ratio will tend towards unity in large, randomly mating populations due to a fitness advantage that accrues in individuals of the rarer sex. This creates a vast excess of sperm over that required to fertilize all available eggs, and intense competition as a result. However, small, inbred populations can experience selection for skewed sex ratios. This is widely appreciated in haplodiploid organisms, in which females can control the sex ratio behaviorally. In this review, we discuss recent research in nematodes that has characterized the mechanisms underlying highly skewed sex ratios in fully diploid systems. These include self-fertile hermaphroditism and the adaptive elimination of sperm competition factors, facultative parthenogenesis, non-Mendelian meiotic oddities involving the sex chromosomes, and environmental sex determination. By connecting sex ratio evolution and sperm biology in surprising ways, these phenomena link two “seminal” contributions of G. A. Parker. 

ABSTRACT The field of developmental biology has declined in prominence in recent decades, with off-shoots from the field becoming more fashionable and highly funded. This has created inequity in discovery and opportunity, partly due to the perception that the field is antiquated or not cutting edge. A ‘think tank’ of scientists from multiple developmental biology-related disciplines came together to define specific challenges in the field that may have inhibited innovation, and to provide tangible solutions to some of the issues facing developmental biology. The community suggestions include a call to the community to help ‘rebrand’ the field, alongside proposals for additional funding apparatuses, frameworks for interdisciplinary innovative collaborations, pedagogical access, improved science communication, increased diversity and inclusion, and equity of resources to provide maximal impact to the community. 

The maintenance of males at intermediate frequencies is an important evolutionary problem. Several species of Caenorhabditis nematodes have evolved a mating system in which selfing hermaphrodites and males coexist. While selfing produces XX hermaphrodites, cross-fertilization produces 50% XO male progeny. Thus, male mating success dictates the sex ratio. Here, we focus on the contribution of the male secreted short (mss) gene family to male mating success, sex ratio, and population growth. The mss family is essential for sperm competitiveness in gonochoristic species, but has been lost in parallel in androdioecious species. Using a transgene to restore mss function to the androdioecious Caenorhabditis briggsae, we examined how mating system and population subdivision influence the fitness of the mss+ genotype. Consistent with theoretical expectations, when mss+ and mss-null (i.e., wild type) genotypes compete, mss+ is positively selected in both mixed-mating and strictly outcrossing situations, though more strongly in the latter. Thus, while sexual mode alone affects the fitness of mss+, it is insufficient to explain its parallel loss. However, in genetically homogenous androdioecious populations, mss+ both increases male frequency and depresses population growth. We propose that the lack of inbreeding depression and the strong subdivision that characterize natural Caenorhabditis populations impose selection on sex ratio that makes loss of mss adaptive after self-fertility evolves.