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COMP-1 promotes competitive advantage of nematode sperm.

Hansen JM, Chavez DR, Stanfield GM - Elife (2015)

Bottom Line: In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts.We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes.Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, United States.

ABSTRACT
Competition among sperm to fertilize oocytes is a ubiquitous feature of sexual reproduction as well as a profoundly important aspect of sexual selection. However, little is known about the cellular mechanisms sperm use to gain competitive advantage or how these mechanisms are regulated genetically. In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts. We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes. Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage. Our results indicate not only that sperm functional traits can influence the outcome of sperm competition, but also that these traits can be modulated in a context-dependent manner depending on the presence of competing sperm.

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The comp-1 mutant has defects in male–male sperm competition.comp-1 male sperm are outcompeted by wild-type male sperm. Wild-type and/or comp-1(gk1149) males were mated sequentially to fog-2 hermaphrodites; first-mated males harbored the transgene mIs11(GFP+). Offspring were scored for GFP, and the percentage of GFP-positive progeny produced 0–16 hr after second-male mating is shown. GFP-marked males show an apparent slight disadvantage, which is observed consistently but is not statistically significant. Lines indicate medians. ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test).DOI:http://dx.doi.org/10.7554/eLife.05423.011
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fig2s1: The comp-1 mutant has defects in male–male sperm competition.comp-1 male sperm are outcompeted by wild-type male sperm. Wild-type and/or comp-1(gk1149) males were mated sequentially to fog-2 hermaphrodites; first-mated males harbored the transgene mIs11(GFP+). Offspring were scored for GFP, and the percentage of GFP-positive progeny produced 0–16 hr after second-male mating is shown. GFP-marked males show an apparent slight disadvantage, which is observed consistently but is not statistically significant. Lines indicate medians. ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test).DOI:http://dx.doi.org/10.7554/eLife.05423.011

Mentions: Since COMP-1 is highly conserved in both male-hermaphrodite and male-female species (Figure 1—figure supplement 1), we hypothesized that comp-1 might function in male–male sperm competition. In the standard laboratory strain of C. elegans (N2), sequential male matings normally show no precedence pattern, i.e., the first and second males to transfer sperm are equally likely to sire offspring (Ward and Carrel, 1979; LaMunyon and Ward, 1998). However, sequential matings of males from different wild-type strains can show preferential sperm usage patterns (LaMunyon and Ward, 1998; Murray et al., 2011), indicating that differences in competitive ability can occur among males in this species. To determine if comp-1 function influences sperm competition in a male vs male context, we performed sequential matings of wild-type and/or comp-1 males to fog-2 mutant hermaphrodites, which fail to produce self sperm and are essentially female (Schedl and Kimble, 1988). To facilitate assignment of paternity, we used strains containing a GFP transgene, mIs11, for either the first or second sets of crosses, and scored offspring for the presence or absence of fluorescence. In control crosses, in which two wild-type males were sequentially mated to hermaphrodites, progeny numbers from the first and second male were variable, but no consistent bias was observed, other than a weak trend in which non-mIs11 males seemed to be slightly favored over mIs11-containing males (Figure 2A, Figure 2—figure supplement 1). Similarly, in sequential matings of two comp-1 males, no precedence order was observed. However, sequential matings of wild-type and comp-1 males resulted in strong precedence for the wild-type sperm, regardless of whether wild-type males were the first or second mates. Notably, comp-1 males showed full fertility in crosses to fog-2 hermaphrodites, which lack their own sperm (Figure 2B). These data indicate that comp-1 males transfer normal numbers of functional sperm, which can be used efficiently when they do not need to compete. However, when other sperm are present, comp-1 sperm show poor usage. Furthermore, the reduced usage of comp-1 sperm is unrelated to the order of their introduction into the hermaphrodite reproductive tract. Rather, male sperm lacking comp-1 function appear to have an intrinsic disadvantage as compared to wild-type sperm.10.7554/eLife.05423.010Figure 2.The comp-1 mutant has defects in male–male sperm competition.


COMP-1 promotes competitive advantage of nematode sperm.

Hansen JM, Chavez DR, Stanfield GM - Elife (2015)

The comp-1 mutant has defects in male–male sperm competition.comp-1 male sperm are outcompeted by wild-type male sperm. Wild-type and/or comp-1(gk1149) males were mated sequentially to fog-2 hermaphrodites; first-mated males harbored the transgene mIs11(GFP+). Offspring were scored for GFP, and the percentage of GFP-positive progeny produced 0–16 hr after second-male mating is shown. GFP-marked males show an apparent slight disadvantage, which is observed consistently but is not statistically significant. Lines indicate medians. ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test).DOI:http://dx.doi.org/10.7554/eLife.05423.011
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Related In: Results  -  Collection

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fig2s1: The comp-1 mutant has defects in male–male sperm competition.comp-1 male sperm are outcompeted by wild-type male sperm. Wild-type and/or comp-1(gk1149) males were mated sequentially to fog-2 hermaphrodites; first-mated males harbored the transgene mIs11(GFP+). Offspring were scored for GFP, and the percentage of GFP-positive progeny produced 0–16 hr after second-male mating is shown. GFP-marked males show an apparent slight disadvantage, which is observed consistently but is not statistically significant. Lines indicate medians. ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test).DOI:http://dx.doi.org/10.7554/eLife.05423.011
Mentions: Since COMP-1 is highly conserved in both male-hermaphrodite and male-female species (Figure 1—figure supplement 1), we hypothesized that comp-1 might function in male–male sperm competition. In the standard laboratory strain of C. elegans (N2), sequential male matings normally show no precedence pattern, i.e., the first and second males to transfer sperm are equally likely to sire offspring (Ward and Carrel, 1979; LaMunyon and Ward, 1998). However, sequential matings of males from different wild-type strains can show preferential sperm usage patterns (LaMunyon and Ward, 1998; Murray et al., 2011), indicating that differences in competitive ability can occur among males in this species. To determine if comp-1 function influences sperm competition in a male vs male context, we performed sequential matings of wild-type and/or comp-1 males to fog-2 mutant hermaphrodites, which fail to produce self sperm and are essentially female (Schedl and Kimble, 1988). To facilitate assignment of paternity, we used strains containing a GFP transgene, mIs11, for either the first or second sets of crosses, and scored offspring for the presence or absence of fluorescence. In control crosses, in which two wild-type males were sequentially mated to hermaphrodites, progeny numbers from the first and second male were variable, but no consistent bias was observed, other than a weak trend in which non-mIs11 males seemed to be slightly favored over mIs11-containing males (Figure 2A, Figure 2—figure supplement 1). Similarly, in sequential matings of two comp-1 males, no precedence order was observed. However, sequential matings of wild-type and comp-1 males resulted in strong precedence for the wild-type sperm, regardless of whether wild-type males were the first or second mates. Notably, comp-1 males showed full fertility in crosses to fog-2 hermaphrodites, which lack their own sperm (Figure 2B). These data indicate that comp-1 males transfer normal numbers of functional sperm, which can be used efficiently when they do not need to compete. However, when other sperm are present, comp-1 sperm show poor usage. Furthermore, the reduced usage of comp-1 sperm is unrelated to the order of their introduction into the hermaphrodite reproductive tract. Rather, male sperm lacking comp-1 function appear to have an intrinsic disadvantage as compared to wild-type sperm.10.7554/eLife.05423.010Figure 2.The comp-1 mutant has defects in male–male sperm competition.

Bottom Line: In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts.We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes.Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage.

View Article: PubMed Central - PubMed

Affiliation: Department of Human Genetics, University of Utah, Salt Lake City, United States.

ABSTRACT
Competition among sperm to fertilize oocytes is a ubiquitous feature of sexual reproduction as well as a profoundly important aspect of sexual selection. However, little is known about the cellular mechanisms sperm use to gain competitive advantage or how these mechanisms are regulated genetically. In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts. We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes. Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage. Our results indicate not only that sperm functional traits can influence the outcome of sperm competition, but also that these traits can be modulated in a context-dependent manner depending on the presence of competing sperm.

Show MeSH
Related in: MedlinePlus