Intense Sperm-Mediated Sexual Conflict Promotes Reproductive Isolation in Caenorhabditis Nematodes

Ting, Janice J.; Woodruff, Gavin C.; Leung, Gemma; Shin, Nara; Cutter, Asher D.; Haag, Eric S.

doi:10.1371/journal.pbio.1001915

Cited by 64 publications

(112 citation statements)

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“…3A, B). In addition, sperm cells were displaced anteriorly comparable to those observed in the F1 hybrids between the two species (Ting et al 2014), suggesting a defect in spermatogenesis. We next performed mating tests to examine whether the sterility is produced by incapability of sperm transfer using MitoTrackerstained sterile males that were mated with C. nigoni virgin female.…”

Section: Resultsmentioning

confidence: 61%

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Ren

et al. 2016

Genome Res.

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Hybrid incompatibility (HI) prevents gene flow between species, thus lying at the heart of speciation genetics. One of the most common HIs is male sterility. Two superficially contradictory observations exist for hybrid male sterility. First, an introgression on the X Chromosome is more likely to produce male sterility than on autosome (so-called large-X theory); second, spermatogenesis genes are enriched on the autosomes but depleted on the X Chromosome (demasculinization of X Chromosome). Analysis of gene expression in Drosophila hybrids suggests a genetic interaction between the X Chromosome and autosomes that is essential for male fertility. However, the prevalence of such an interaction and its underlying mechanism remain largely unknown. Here we examine the interaction in nematode species by contrasting the expression of both coding genes and transposable elements (TEs) between hybrid sterile males and its parental nematode males. We use two lines of hybrid sterile males, each carrying an independent introgression fragment from Caenorhabditis briggsae X Chromosome in an otherwise Caenorhabditis nigoni background, which demonstrate similar defects in spermatogenesis. We observe a similar pattern of down-regulated genes that are specific for spermatogenesis between the two hybrids. Importantly, the down-regulated genes caused by the X Chromosome introgressions show a significant enrichment on the autosomes, supporting an epistatic interaction between the X Chromosome and autosomes. We investigate the underlying mechanism of the interaction by measuring small RNAs and find that a subset of 22G RNAs specifically targeting the down-regulated spermatogenesis genes is significantly up-regulated in hybrids, suggesting that perturbation of small RNA-mediated regulation may contribute to the X-autosome interaction.

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Section: Resultsmentioning

confidence: 61%

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Ren

et al. 2016

Genome Res.

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“…They remain partially interfertile, yet have numerous genetic and reproductive incompatibilities (9, 15, 17–19). To compare their genomes , we assembled the C. nigoni genome from 20-kb Pacific Biosciences (PacBio) and Illumina short-read libraries (table S1; (20)).…”

Section: Resultsmentioning

confidence: 99%

“…Unlike comp-1, which encodes a kinase required for male versus hermaphrodite sperm competition in C. elegans (37), and which is conserved regardless of mating system, we found mss orthologs only in outcrossing species. In interspecies matings, sperm from males of outcrossing species rapidly invade the ovaries and body cavities of selfing hermaphrodites, sterilizing or killing them (9). This cryptic toxicity of outcrossing sperm is likely due to ongoing sexual selection in outcrossing species.…”

Section: Discussionmentioning

confidence: 99%

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Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

Yin

Schwarz

Thomas

et al. 2018

Science

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To reveal impacts of sexual mode on genome content, we compared chromosome-scale assemblies of the outcrossing nematode Caenorhabditis nigoni to its self-fertile sibling species, C. briggsae. C. nigoni’s genome resembles outcrossing relatives, but encodes 31% more protein-coding genes than C. briggsae. C. nigoni genes lacking C. briggsae orthologs were disproportionately small and male-biased in expression. These include the male secreted short (mss) gene family, which encodes sperm surface glycoproteins conserved only in outcrossing species. Sperm from mss-null males of outcrossing C. remanei failed to compete with wild-type sperm, despite normal fertility in non-competitive mating. Restoring mss to C. briggsae males was sufficient to enhance sperm competitiveness. Thus, sex has a pervasive influence on genome content that can be used to identify sperm competition factors.

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“…It is also unclear whether these changes provide any benefit to the male mating partner or its offspring. A clear danger of mating has been demonstrated in other species of Caenorhabditis, however; for example, C. nigoni males have been shown to sterilize and kill hermaphrodites and females of other species through the action of their sperm (40).…”

Section: Discussionmentioning

confidence: 99%

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Leighton

Choe

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Males of the androdioecious species Caenorhabditis elegans are more likely to attempt to mate with and successfully inseminate C. elegans hermaphrodites that do not concurrently harbor sperm. Although a small number of genes have been implicated in this effect, the mechanism by which it arises remains unknown. In the context of the battle of the sexes, it is also unknown whether this effect is to the benefit of the male, the hermaphrodite, or both. We report that successful contact between mature sperm and oocyte in the C. elegans gonad at the start of fertilization causes the oocyte to release a signal that is transmitted to somatic cells in its mother, with the ultimate effect of reducing her attractiveness to males. Changes in hermaphrodite attractiveness are tied to the production of a volatile pheromone, the first such pheromone described in C. elegans.fertilization | sex pheromones | egg-soma communication I ts properties of self-fertilization and rapid generation, along with its extensive library of mutants, make Caenorhabditis elegans an excellent system in which to study reproductive events. The generation time of C. elegans is under 3 d, and a single hermaphroditic worm can use its sperm to fertilize its own eggs, without the need for mating (1). C. elegans and related nematodes have a robust sperm sensation pathway that limits unfruitful oocyte maturation and ovulation (2). Both self-sperm and nonself-sperm secrete protein ligands, known as major sperm proteins (MSPs), that activate signal transduction pathways in both unfertilized oocytes, leading to activation of mitogen-activated protein kinase (MPK-1), and the somatic gonad, involving transcription factor CEH-18. The result of this signaling is the release of oocytes from prophase I arrest and the ovulation of unarrested oocytes into the uterus (3, 4).Several behaviors of female and hermaphroditic nematodes have been demonstrated to correlate with either the presence of sperm or the recentness of mating. C. elegans hermaphrodites that have exhausted their supply of self-sperm are more likely to elicit a mating response from males of their species, and less likely to resist an attempted mating. Mutant C. elegans hermaphrodites that develop without self-sperm also elicit more mating attempts, and this increase in attractiveness vanishes after a successful mating (5, 6). In the gonochoristic species Caenorhabditis brenneri and Caenorhabditis remanei, males are attracted to a volatile pheromone produced only by females that have not recently mated (7). The mechanisms that link these behaviors to sperm status remain unknown.Pheromones have been shown to exist in dozens of nematode species (8-10) and have been positively identified in several, including C. elegans (11-14). Although HPLC-MS studies have led to the identification of more than 140 pheromones and pheromone-related metabolites in C. elegans (15), little is known about how production of such pheromones is regulated. Life stage and environmental conditions have been shown to affect pheromone o...

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Intense Sperm-Mediated Sexual Conflict Promotes Reproductive Isolation in Caenorhabditis Nematodes

Abstract: Sperm from other species invade female tissues to cause sterility and death, helping to keep nematode species boundaries intact.

Cited by 64 publications

References 78 publications

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

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