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Mating damages the cuticle of C. elegans hermaphrodites.

Woodruff GC, Knauss CM, Maugel TK, Haag ES - PLoS ONE (2014)

Bottom Line: Lifespan costs to reproduction are common across multiple species, and such costs could potentially arise through a number of mechanisms.In the nematode Caenorhabditis elegans, it has been suggested that part of the lifespan cost to hermaphrodites from mating results from physical damage owing to the act of copulation itself.We further discuss our results within the context of recent studies linking the lifespan cost to mating in C. elegans hermaphrodites to male secretions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Maryland, College Park, Maryland, United States of America; Forest Pathology Laboratory, Forestry and Forest Products Research Institute, Tsukuba, Ibaraki, Japan.

ABSTRACT
Lifespan costs to reproduction are common across multiple species, and such costs could potentially arise through a number of mechanisms. In the nematode Caenorhabditis elegans, it has been suggested that part of the lifespan cost to hermaphrodites from mating results from physical damage owing to the act of copulation itself. Here, we examine whether mating damages the surface of the hermaphrodite cuticle via scanning electron microscopy. It is found that mated hermaphrodites suffered delamination of cuticle layers surrounding the vulva, and that the incidence of such damage depends on genetic background. Unmated hermaphrodites demonstrated almost no such damage, even when cultured in soil with potentially abrasive particles. Thus, a consequence of mating for C. elegans hermaphrodites is physical cuticle damage. These experiments did not assess the consequences of cuticle damage for lifespan, and the biological significance of this damage remains unclear. We further discuss our results within the context of recent studies linking the lifespan cost to mating in C. elegans hermaphrodites to male secretions.

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Related in: MedlinePlus

Soil conditions do not cause cuticle damage.SEM images of hermaphrodites grown in soil plate conditions. (A) Low- (left) and high-magnification (right) images of a worm grown for five days in soil, showing pristine ultrastructure of the cuticle. The three parallel alae (ridges running transversely across the cuticle) are clearly visible in the high-magnification view. (B) Soil conditions also do not damage cuticle surrounding the vulva. Two representative specimens are shown. Scales bars represent 100 microns in A and 10 microns in B.
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pone-0104456-g002: Soil conditions do not cause cuticle damage.SEM images of hermaphrodites grown in soil plate conditions. (A) Low- (left) and high-magnification (right) images of a worm grown for five days in soil, showing pristine ultrastructure of the cuticle. The three parallel alae (ridges running transversely across the cuticle) are clearly visible in the high-magnification view. (B) Soil conditions also do not damage cuticle surrounding the vulva. Two representative specimens are shown. Scales bars represent 100 microns in A and 10 microns in B.

Mentions: The marked increase in cuticle damage due to mating led us to examine whether other stresses may also promote such damage. Laboratory conditions are quite different from the natural ecological context of C. elegans[31]. Caenorhabditis is thought to proliferate on rotting fruit adjacent to soil [32], so we examined worms cultured in a bacteria-soil mixture atop standard agar medium for five days (see Methods). However, hermaphrodites on these “dirt plates” were not obviously abraded (Figure 2A, n = 12), and showed no discernable difference in overall cuticle morphology from hermaphrodites grown on standard media (data not shown). Moreover, soil-cultured hermaphrodites lacked any apparent cuticle damage around the vulva (Figure 2B; n = 7), suggesting that the vulva is not particularly susceptible to such damage. Thus, mating may be particularly harmful for hermaphrodites, as traversing through potentially harsh conditions appears to not promote such physical damage.


Mating damages the cuticle of C. elegans hermaphrodites.

Woodruff GC, Knauss CM, Maugel TK, Haag ES - PLoS ONE (2014)

Soil conditions do not cause cuticle damage.SEM images of hermaphrodites grown in soil plate conditions. (A) Low- (left) and high-magnification (right) images of a worm grown for five days in soil, showing pristine ultrastructure of the cuticle. The three parallel alae (ridges running transversely across the cuticle) are clearly visible in the high-magnification view. (B) Soil conditions also do not damage cuticle surrounding the vulva. Two representative specimens are shown. Scales bars represent 100 microns in A and 10 microns in B.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4126722&req=5

pone-0104456-g002: Soil conditions do not cause cuticle damage.SEM images of hermaphrodites grown in soil plate conditions. (A) Low- (left) and high-magnification (right) images of a worm grown for five days in soil, showing pristine ultrastructure of the cuticle. The three parallel alae (ridges running transversely across the cuticle) are clearly visible in the high-magnification view. (B) Soil conditions also do not damage cuticle surrounding the vulva. Two representative specimens are shown. Scales bars represent 100 microns in A and 10 microns in B.
Mentions: The marked increase in cuticle damage due to mating led us to examine whether other stresses may also promote such damage. Laboratory conditions are quite different from the natural ecological context of C. elegans[31]. Caenorhabditis is thought to proliferate on rotting fruit adjacent to soil [32], so we examined worms cultured in a bacteria-soil mixture atop standard agar medium for five days (see Methods). However, hermaphrodites on these “dirt plates” were not obviously abraded (Figure 2A, n = 12), and showed no discernable difference in overall cuticle morphology from hermaphrodites grown on standard media (data not shown). Moreover, soil-cultured hermaphrodites lacked any apparent cuticle damage around the vulva (Figure 2B; n = 7), suggesting that the vulva is not particularly susceptible to such damage. Thus, mating may be particularly harmful for hermaphrodites, as traversing through potentially harsh conditions appears to not promote such physical damage.

Bottom Line: Lifespan costs to reproduction are common across multiple species, and such costs could potentially arise through a number of mechanisms.In the nematode Caenorhabditis elegans, it has been suggested that part of the lifespan cost to hermaphrodites from mating results from physical damage owing to the act of copulation itself.We further discuss our results within the context of recent studies linking the lifespan cost to mating in C. elegans hermaphrodites to male secretions.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Maryland, College Park, Maryland, United States of America; Forest Pathology Laboratory, Forestry and Forest Products Research Institute, Tsukuba, Ibaraki, Japan.

ABSTRACT
Lifespan costs to reproduction are common across multiple species, and such costs could potentially arise through a number of mechanisms. In the nematode Caenorhabditis elegans, it has been suggested that part of the lifespan cost to hermaphrodites from mating results from physical damage owing to the act of copulation itself. Here, we examine whether mating damages the surface of the hermaphrodite cuticle via scanning electron microscopy. It is found that mated hermaphrodites suffered delamination of cuticle layers surrounding the vulva, and that the incidence of such damage depends on genetic background. Unmated hermaphrodites demonstrated almost no such damage, even when cultured in soil with potentially abrasive particles. Thus, a consequence of mating for C. elegans hermaphrodites is physical cuticle damage. These experiments did not assess the consequences of cuticle damage for lifespan, and the biological significance of this damage remains unclear. We further discuss our results within the context of recent studies linking the lifespan cost to mating in C. elegans hermaphrodites to male secretions.

Show MeSH
Related in: MedlinePlus