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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.
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Evolution of sex ratio through gene loss
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.
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- Award ID(s):
- 1755379
- PAR ID:
- 10109702
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Volume:
- 116
- Issue:
- 26
- ISSN:
- 1091-6490
- Page Range / eLocation ID:
- 12919–12924
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/www.pnas.org/cgi/doi/10.1073/pnas.1903925116
