Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes

Sexual interactions have a potent influence on health in several species, including mammals. Previous work in C. elegans identified strategies used by males to accelerate the demise of the opposite sex (hermaphrodites). But whether hermaphrodites evolved counter-strategies against males remains unkn...

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Main Authors: Lauren N Booth, Travis J Maures, Robin W Yeo, Cindy Tantilert, Anne Brunet
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/46418
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author Lauren N Booth
Travis J Maures
Robin W Yeo
Cindy Tantilert
Anne Brunet
author_facet Lauren N Booth
Travis J Maures
Robin W Yeo
Cindy Tantilert
Anne Brunet
author_sort Lauren N Booth
collection DOAJ
description Sexual interactions have a potent influence on health in several species, including mammals. Previous work in C. elegans identified strategies used by males to accelerate the demise of the opposite sex (hermaphrodites). But whether hermaphrodites evolved counter-strategies against males remains unknown. Here we discover that young C. elegans hermaphrodites are remarkably resistant to brief sexual encounters with males, whereas older hermaphrodites succumb prematurely. Surprisingly, it is not their youthfulness that protects young hermaphrodites, but the fact that they have self-sperm. The beneficial effect of self-sperm is mediated by a sperm-sensing pathway acting on the soma rather than by fertilization. Activation of this pathway in females triggers protection from the negative impact of males. Interestingly, the role of self-sperm in protecting against the detrimental effects of males evolved independently in hermaphroditic nematodes. Endogenous strategies to delay the negative effect of mating may represent a key evolutionary innovation to maximize reproductive success.
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spelling doaj.art-99deafde9a784bc2b10fd3445a4776482022-12-22T02:03:13ZengeLife Sciences Publications LtdeLife2050-084X2019-07-01810.7554/eLife.46418Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodesLauren N Booth0https://orcid.org/0000-0003-3072-6235Travis J Maures1Robin W Yeo2Cindy Tantilert3Anne Brunet4https://orcid.org/0000-0002-4608-6845Department of Genetics, Stanford University, Stanford, United StatesDepartment of Genetics, Stanford University, Stanford, United StatesDepartment of Genetics, Stanford University, Stanford, United StatesDepartment of Genetics, Stanford University, Stanford, United StatesDepartment of Genetics, Stanford University, Stanford, United States; Glenn Laboratories for the Biology of Aging at Stanford University, Stanford, United StatesSexual interactions have a potent influence on health in several species, including mammals. Previous work in C. elegans identified strategies used by males to accelerate the demise of the opposite sex (hermaphrodites). But whether hermaphrodites evolved counter-strategies against males remains unknown. Here we discover that young C. elegans hermaphrodites are remarkably resistant to brief sexual encounters with males, whereas older hermaphrodites succumb prematurely. Surprisingly, it is not their youthfulness that protects young hermaphrodites, but the fact that they have self-sperm. The beneficial effect of self-sperm is mediated by a sperm-sensing pathway acting on the soma rather than by fertilization. Activation of this pathway in females triggers protection from the negative impact of males. Interestingly, the role of self-sperm in protecting against the detrimental effects of males evolved independently in hermaphroditic nematodes. Endogenous strategies to delay the negative effect of mating may represent a key evolutionary innovation to maximize reproductive success.https://elifesciences.org/articles/46418C. briggsaeself-spermhermaphrodite evolutionagingmating-induced deathsexual interactions
spellingShingle Lauren N Booth
Travis J Maures
Robin W Yeo
Cindy Tantilert
Anne Brunet
Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
eLife
C. briggsae
self-sperm
hermaphrodite evolution
aging
mating-induced death
sexual interactions
title Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
title_full Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
title_fullStr Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
title_full_unstemmed Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
title_short Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
title_sort self sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
topic C. briggsae
self-sperm
hermaphrodite evolution
aging
mating-induced death
sexual interactions
url https://elifesciences.org/articles/46418
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