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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 can crawl and be activated in vitro.(A) comp-1 sperm can crawl at wild-type velocities in vitro. Wild-type and comp-1(gk1149) spermatids were treated with TEA for 30 min and velocity was obtained from time-lapse images collected every 30 s. As we observed a high level of variability among different samples for each genotype, the range of observed values is shown using a box-and-whiskers plot. For each genotype, n = 5–6 samples, 65–130 cells. (B) comp-1 sperm activate in Pronase. Wild-type and comp-1(gk1149) spermatids were treated with Pronase for 30 min and scored for activation based on the presence or absence of a pseudopod. Error bars, 95% confidence intervals.DOI:http://dx.doi.org/10.7554/eLife.05423.018
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fig7s1: comp-1 sperm can crawl and be activated in vitro.(A) comp-1 sperm can crawl at wild-type velocities in vitro. Wild-type and comp-1(gk1149) spermatids were treated with TEA for 30 min and velocity was obtained from time-lapse images collected every 30 s. As we observed a high level of variability among different samples for each genotype, the range of observed values is shown using a box-and-whiskers plot. For each genotype, n = 5–6 samples, 65–130 cells. (B) comp-1 sperm activate in Pronase. Wild-type and comp-1(gk1149) spermatids were treated with Pronase for 30 min and scored for activation based on the presence or absence of a pseudopod. Error bars, 95% confidence intervals.DOI:http://dx.doi.org/10.7554/eLife.05423.018

Mentions: To further analyze the motility of comp-1 mutant sperm, we dissected spermatids, treated them with the known in vitro activators TEA (triethanolamine, a weak base) or Pronase (a protease mixture) (Ward et al., 1983; Shakes and Ward, 1989), and sought to measure the velocities of cells crawling on glass slides (Nelson et al., 1982). comp-1 sperm activated in TEA had extended pseudopods and were capable of crawling at speeds similar to those of wild-type cells (Figure 7B–D, Figure 7—figure supplement 1A). comp-1 sperm treated with Pronase activated at rates similar to the wild type (Figure 7—figure supplement 1B), based on the presence of a pseudopod in the majority of cells. However, the shapes of comp-1 cells were markedly different from wild-type (Figure 7E–F and data not shown). Quantification of pseudopod length, using an aspect ratio measurement to normalize for variation in cell size (Batchelder et al., 2011), confirmed that Pronase-treated comp-1 cells were significantly shorter than either wild-type or TEA-treated comp-1 cells (Figure 7B). Since Pronase-treated comp-1 cells contained distinct cell body and pseudopod regions, with normal localization of organelles (Figure 5, Figure 7, and data not shown), it is likely that these cells were polarized but failed to extend their pseudopods appropriately. Similar to other amoeboid cells, locomotion of nematode sperm depends on protrusion of the lamellipodium-like pseudopod, adhesion to substrate, and retraction of the cell body (Roberts and Stewart, 2000; Bottino et al., 2002). Pseudopod extension defects would be expected to result in altered locomotion and/or interactions with the hermaphrodite reproductive tract, which in turn should affect migration to and occupation of the spermathecae.


COMP-1 promotes competitive advantage of nematode sperm.

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

comp-1 sperm can crawl and be activated in vitro.(A) comp-1 sperm can crawl at wild-type velocities in vitro. Wild-type and comp-1(gk1149) spermatids were treated with TEA for 30 min and velocity was obtained from time-lapse images collected every 30 s. As we observed a high level of variability among different samples for each genotype, the range of observed values is shown using a box-and-whiskers plot. For each genotype, n = 5–6 samples, 65–130 cells. (B) comp-1 sperm activate in Pronase. Wild-type and comp-1(gk1149) spermatids were treated with Pronase for 30 min and scored for activation based on the presence or absence of a pseudopod. Error bars, 95% confidence intervals.DOI:http://dx.doi.org/10.7554/eLife.05423.018
© Copyright Policy
Related In: Results  -  Collection

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

fig7s1: comp-1 sperm can crawl and be activated in vitro.(A) comp-1 sperm can crawl at wild-type velocities in vitro. Wild-type and comp-1(gk1149) spermatids were treated with TEA for 30 min and velocity was obtained from time-lapse images collected every 30 s. As we observed a high level of variability among different samples for each genotype, the range of observed values is shown using a box-and-whiskers plot. For each genotype, n = 5–6 samples, 65–130 cells. (B) comp-1 sperm activate in Pronase. Wild-type and comp-1(gk1149) spermatids were treated with Pronase for 30 min and scored for activation based on the presence or absence of a pseudopod. Error bars, 95% confidence intervals.DOI:http://dx.doi.org/10.7554/eLife.05423.018
Mentions: To further analyze the motility of comp-1 mutant sperm, we dissected spermatids, treated them with the known in vitro activators TEA (triethanolamine, a weak base) or Pronase (a protease mixture) (Ward et al., 1983; Shakes and Ward, 1989), and sought to measure the velocities of cells crawling on glass slides (Nelson et al., 1982). comp-1 sperm activated in TEA had extended pseudopods and were capable of crawling at speeds similar to those of wild-type cells (Figure 7B–D, Figure 7—figure supplement 1A). comp-1 sperm treated with Pronase activated at rates similar to the wild type (Figure 7—figure supplement 1B), based on the presence of a pseudopod in the majority of cells. However, the shapes of comp-1 cells were markedly different from wild-type (Figure 7E–F and data not shown). Quantification of pseudopod length, using an aspect ratio measurement to normalize for variation in cell size (Batchelder et al., 2011), confirmed that Pronase-treated comp-1 cells were significantly shorter than either wild-type or TEA-treated comp-1 cells (Figure 7B). Since Pronase-treated comp-1 cells contained distinct cell body and pseudopod regions, with normal localization of organelles (Figure 5, Figure 7, and data not shown), it is likely that these cells were polarized but failed to extend their pseudopods appropriately. Similar to other amoeboid cells, locomotion of nematode sperm depends on protrusion of the lamellipodium-like pseudopod, adhesion to substrate, and retraction of the cell body (Roberts and Stewart, 2000; Bottino et al., 2002). Pseudopod extension defects would be expected to result in altered locomotion and/or interactions with the hermaphrodite reproductive tract, which in turn should affect migration to and occupation of the spermathecae.

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