Limits...
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.

Show MeSH

Related in: MedlinePlus

comp-1 male sperm have long-term precedence defects.(A) Crosses with comp-1 males result in a low percentage of cross progeny. (B) The number of cross progeny sired by comp-1 increases at late time points. (C) Crosses with comp-1 males do not suppress production of self progeny. Purple line indicates self progeny of unmated hermaphrodites. (D) Crosses with comp-1 males result in decreased progeny numbers as compared to those with wild-type males. (A–D) Males were crossed to dpy-4 hermaphrodites for 16 hr (gray line); progeny were collected throughout the recipients' reproductive lifespans and scored as self or cross progeny. All graphs are from a single data set that is representative of three repeats. For B–D, cumulative progeny numbers are shown. (E) comp-1 male sperm are used at wild-type levels in crosses to sperm-depleted hermaphrodites. Males were crossed to staged dpy-4 recipients for 24 hr and progeny generated during the mating period were scored as self or cross progeny. ‘No. remaining sperm’ indicates the number of self sperm present within recipients at each stage, inferred from brood counts of unmated dpy-4 hermaphrodites performed in parallel. Data points indicate averages; error bars, 95% confidence intervals. **, p < 0.01; ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test, comparing wild-type to each comp-1 mutant).DOI:http://dx.doi.org/10.7554/eLife.05423.012
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4400581&req=5

fig3: comp-1 male sperm have long-term precedence defects.(A) Crosses with comp-1 males result in a low percentage of cross progeny. (B) The number of cross progeny sired by comp-1 increases at late time points. (C) Crosses with comp-1 males do not suppress production of self progeny. Purple line indicates self progeny of unmated hermaphrodites. (D) Crosses with comp-1 males result in decreased progeny numbers as compared to those with wild-type males. (A–D) Males were crossed to dpy-4 hermaphrodites for 16 hr (gray line); progeny were collected throughout the recipients' reproductive lifespans and scored as self or cross progeny. All graphs are from a single data set that is representative of three repeats. For B–D, cumulative progeny numbers are shown. (E) comp-1 male sperm are used at wild-type levels in crosses to sperm-depleted hermaphrodites. Males were crossed to staged dpy-4 recipients for 24 hr and progeny generated during the mating period were scored as self or cross progeny. ‘No. remaining sperm’ indicates the number of self sperm present within recipients at each stage, inferred from brood counts of unmated dpy-4 hermaphrodites performed in parallel. Data points indicate averages; error bars, 95% confidence intervals. **, p < 0.01; ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test, comparing wild-type to each comp-1 mutant).DOI:http://dx.doi.org/10.7554/eLife.05423.012

Mentions: To investigate the importance of comp-1 activity for male reproductive success, we sought to determine the nature of the competitive defect of comp-1 mutant sperm. In particular, we wished to know if comp-1 sperm were lost or remained active within the gonads of hermaphrodites. To address this question, we assayed the long-term kinetics of usage of comp-1 male sperm within hermaphrodites. We crossed wild-type or comp-1 males to dpy-4 hermaphrodites for 16 hr, transferred the recipients at 12-hr intervals until they ceased egg laying, and counted the total number of self and cross progeny at each time point. Wild-type male sperm usage increased rapidly after mating (Figure 3A), consistent with previous evidence that male sperm are used preferentially over hermaphrodite self sperm (Ward, 1977; Ward and Carrel, 1979; LaMunyon and Ward, 1995). However, comp-1 mutant males sired almost no progeny until late in the hermaphrodite lifespan (Figure 3A,B). Furthermore, while mating with wild-type males suppressed usage of self sperm, mating with comp-1 males had no effect on self-progeny production (Figure 3C). Thus, comp-1 males show severe long-term defects in their ability to produce offspring after mating, and hermaphrodites that mate with comp-1 males produce a decreased number of total offspring (Figure 3D). However, although they are initially unsuccessful in fertilizing eggs, at least some comp-1 sperm are eventually used, indicating that they can remain in the reproductive tract.10.7554/eLife.05423.012Figure 3.comp-1 male sperm have long-term precedence defects.


COMP-1 promotes competitive advantage of nematode sperm.

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

comp-1 male sperm have long-term precedence defects.(A) Crosses with comp-1 males result in a low percentage of cross progeny. (B) The number of cross progeny sired by comp-1 increases at late time points. (C) Crosses with comp-1 males do not suppress production of self progeny. Purple line indicates self progeny of unmated hermaphrodites. (D) Crosses with comp-1 males result in decreased progeny numbers as compared to those with wild-type males. (A–D) Males were crossed to dpy-4 hermaphrodites for 16 hr (gray line); progeny were collected throughout the recipients' reproductive lifespans and scored as self or cross progeny. All graphs are from a single data set that is representative of three repeats. For B–D, cumulative progeny numbers are shown. (E) comp-1 male sperm are used at wild-type levels in crosses to sperm-depleted hermaphrodites. Males were crossed to staged dpy-4 recipients for 24 hr and progeny generated during the mating period were scored as self or cross progeny. ‘No. remaining sperm’ indicates the number of self sperm present within recipients at each stage, inferred from brood counts of unmated dpy-4 hermaphrodites performed in parallel. Data points indicate averages; error bars, 95% confidence intervals. **, p < 0.01; ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test, comparing wild-type to each comp-1 mutant).DOI:http://dx.doi.org/10.7554/eLife.05423.012
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400581&req=5

fig3: comp-1 male sperm have long-term precedence defects.(A) Crosses with comp-1 males result in a low percentage of cross progeny. (B) The number of cross progeny sired by comp-1 increases at late time points. (C) Crosses with comp-1 males do not suppress production of self progeny. Purple line indicates self progeny of unmated hermaphrodites. (D) Crosses with comp-1 males result in decreased progeny numbers as compared to those with wild-type males. (A–D) Males were crossed to dpy-4 hermaphrodites for 16 hr (gray line); progeny were collected throughout the recipients' reproductive lifespans and scored as self or cross progeny. All graphs are from a single data set that is representative of three repeats. For B–D, cumulative progeny numbers are shown. (E) comp-1 male sperm are used at wild-type levels in crosses to sperm-depleted hermaphrodites. Males were crossed to staged dpy-4 recipients for 24 hr and progeny generated during the mating period were scored as self or cross progeny. ‘No. remaining sperm’ indicates the number of self sperm present within recipients at each stage, inferred from brood counts of unmated dpy-4 hermaphrodites performed in parallel. Data points indicate averages; error bars, 95% confidence intervals. **, p < 0.01; ***, p < 0.001; ns, not significant (Kolmogorov–Smirnov test, comparing wild-type to each comp-1 mutant).DOI:http://dx.doi.org/10.7554/eLife.05423.012
Mentions: To investigate the importance of comp-1 activity for male reproductive success, we sought to determine the nature of the competitive defect of comp-1 mutant sperm. In particular, we wished to know if comp-1 sperm were lost or remained active within the gonads of hermaphrodites. To address this question, we assayed the long-term kinetics of usage of comp-1 male sperm within hermaphrodites. We crossed wild-type or comp-1 males to dpy-4 hermaphrodites for 16 hr, transferred the recipients at 12-hr intervals until they ceased egg laying, and counted the total number of self and cross progeny at each time point. Wild-type male sperm usage increased rapidly after mating (Figure 3A), consistent with previous evidence that male sperm are used preferentially over hermaphrodite self sperm (Ward, 1977; Ward and Carrel, 1979; LaMunyon and Ward, 1995). However, comp-1 mutant males sired almost no progeny until late in the hermaphrodite lifespan (Figure 3A,B). Furthermore, while mating with wild-type males suppressed usage of self sperm, mating with comp-1 males had no effect on self-progeny production (Figure 3C). Thus, comp-1 males show severe long-term defects in their ability to produce offspring after mating, and hermaphrodites that mate with comp-1 males produce a decreased number of total offspring (Figure 3D). However, although they are initially unsuccessful in fertilizing eggs, at least some comp-1 sperm are eventually used, indicating that they can remain in the reproductive tract.10.7554/eLife.05423.012Figure 3.comp-1 male sperm have long-term precedence defects.

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