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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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comp-1 sperm have defects in migration and spermathecal accumulation.(A) Schematic of hermaphrodite gonad arm showing zones used to quantify sperm position. (B, C) Localization of wild-type (B) and comp-1(gk1149) (C) Mitotracker-labeled male sperm 1–1.5 hr after transfer to hermaphrodites. Percentage of total male sperm is shown. (D, E) Localization of jnSi118[GFP::H2B] male sperm 12 hr (D) and 24 hr (E) after transfer to hermaphrodites. Percentage of male sperm in the focal plane with maximum sperm in the spermatheca is shown. (F) Localization of hermaphrodite self sperm in 24 hr post-L4 unmated hermaphrodites. Animals were stained with DAPI to facilitate counting of sperm cells. Percentage of total hermaphrodite sperm is shown. Error bars, 95% confidence intervals. *, p < 0.05; **, p < 0.01; ***, p < 0.001; Student's t test.DOI:http://dx.doi.org/10.7554/eLife.05423.016
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fig6: comp-1 sperm have defects in migration and spermathecal accumulation.(A) Schematic of hermaphrodite gonad arm showing zones used to quantify sperm position. (B, C) Localization of wild-type (B) and comp-1(gk1149) (C) Mitotracker-labeled male sperm 1–1.5 hr after transfer to hermaphrodites. Percentage of total male sperm is shown. (D, E) Localization of jnSi118[GFP::H2B] male sperm 12 hr (D) and 24 hr (E) after transfer to hermaphrodites. Percentage of male sperm in the focal plane with maximum sperm in the spermatheca is shown. (F) Localization of hermaphrodite self sperm in 24 hr post-L4 unmated hermaphrodites. Animals were stained with DAPI to facilitate counting of sperm cells. Percentage of total hermaphrodite sperm is shown. Error bars, 95% confidence intervals. *, p < 0.05; **, p < 0.01; ***, p < 0.001; Student's t test.DOI:http://dx.doi.org/10.7554/eLife.05423.016

Mentions: In C. elegans, sperm are stored and fertilization occurs within the spermathecae (Ward and Carrel, 1979). Transferred male sperm must migrate through the uterus and into the spermathecae to be eligible to fertilize oocytes, and male sperm have been observed to displace hermaphrodite sperm from the walls of these structures (Ward and Carrel, 1979). We thus examined the ability of comp-1 mutant sperm to migrate toward and access the spermathecae. We crossed unlabeled hermaphrodites to males either labeled with Mitotracker dye (Kubagawa et al., 2006; Stanfield and Villeneuve, 2006) or expressing a sperm H2B::GFP reporter, and then examined male sperm positioning at different time points after transfer to the hermaphrodite reproductive tract. Similar to previously reported analyses of sperm migration (Kubagawa et al., 2006), we divided each proximal gonad arm into four regions: zone 1, near the sperm entry point at the vulva; zone 2, within the uterus; zone 3, the region near the spermatheca; and the spermatheca itself (Figure 6A).10.7554/eLife.05423.016Figure 6.comp-1 sperm have defects in migration and spermathecal accumulation.


COMP-1 promotes competitive advantage of nematode sperm.

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

comp-1 sperm have defects in migration and spermathecal accumulation.(A) Schematic of hermaphrodite gonad arm showing zones used to quantify sperm position. (B, C) Localization of wild-type (B) and comp-1(gk1149) (C) Mitotracker-labeled male sperm 1–1.5 hr after transfer to hermaphrodites. Percentage of total male sperm is shown. (D, E) Localization of jnSi118[GFP::H2B] male sperm 12 hr (D) and 24 hr (E) after transfer to hermaphrodites. Percentage of male sperm in the focal plane with maximum sperm in the spermatheca is shown. (F) Localization of hermaphrodite self sperm in 24 hr post-L4 unmated hermaphrodites. Animals were stained with DAPI to facilitate counting of sperm cells. Percentage of total hermaphrodite sperm is shown. Error bars, 95% confidence intervals. *, p < 0.05; **, p < 0.01; ***, p < 0.001; Student's t test.DOI:http://dx.doi.org/10.7554/eLife.05423.016
© Copyright Policy
Related In: Results  -  Collection

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fig6: comp-1 sperm have defects in migration and spermathecal accumulation.(A) Schematic of hermaphrodite gonad arm showing zones used to quantify sperm position. (B, C) Localization of wild-type (B) and comp-1(gk1149) (C) Mitotracker-labeled male sperm 1–1.5 hr after transfer to hermaphrodites. Percentage of total male sperm is shown. (D, E) Localization of jnSi118[GFP::H2B] male sperm 12 hr (D) and 24 hr (E) after transfer to hermaphrodites. Percentage of male sperm in the focal plane with maximum sperm in the spermatheca is shown. (F) Localization of hermaphrodite self sperm in 24 hr post-L4 unmated hermaphrodites. Animals were stained with DAPI to facilitate counting of sperm cells. Percentage of total hermaphrodite sperm is shown. Error bars, 95% confidence intervals. *, p < 0.05; **, p < 0.01; ***, p < 0.001; Student's t test.DOI:http://dx.doi.org/10.7554/eLife.05423.016
Mentions: In C. elegans, sperm are stored and fertilization occurs within the spermathecae (Ward and Carrel, 1979). Transferred male sperm must migrate through the uterus and into the spermathecae to be eligible to fertilize oocytes, and male sperm have been observed to displace hermaphrodite sperm from the walls of these structures (Ward and Carrel, 1979). We thus examined the ability of comp-1 mutant sperm to migrate toward and access the spermathecae. We crossed unlabeled hermaphrodites to males either labeled with Mitotracker dye (Kubagawa et al., 2006; Stanfield and Villeneuve, 2006) or expressing a sperm H2B::GFP reporter, and then examined male sperm positioning at different time points after transfer to the hermaphrodite reproductive tract. Similar to previously reported analyses of sperm migration (Kubagawa et al., 2006), we divided each proximal gonad arm into four regions: zone 1, near the sperm entry point at the vulva; zone 2, within the uterus; zone 3, the region near the spermatheca; and the spermatheca itself (Figure 6A).10.7554/eLife.05423.016Figure 6.comp-1 sperm have defects in migration and spermathecal accumulation.

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