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...
Main Authors: | , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2019-07-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/46418 |
_version_ | 1818023962648510464 |
---|---|
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. |
first_indexed | 2024-12-10T03:52:39Z |
format | Article |
id | doaj.art-99deafde9a784bc2b10fd3445a477648 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-12-10T03:52:39Z |
publishDate | 2019-07-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT laurennbooth selfsperminduceresistancetothedetrimentaleffectsofsexualencounterswithmalesinhermaphroditicnematodes AT travisjmaures selfsperminduceresistancetothedetrimentaleffectsofsexualencounterswithmalesinhermaphroditicnematodes AT robinwyeo selfsperminduceresistancetothedetrimentaleffectsofsexualencounterswithmalesinhermaphroditicnematodes AT cindytantilert selfsperminduceresistancetothedetrimentaleffectsofsexualencounterswithmalesinhermaphroditicnematodes AT annebrunet selfsperminduceresistancetothedetrimentaleffectsofsexualencounterswithmalesinhermaphroditicnematodes |