Cargando…

Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila

Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the...

Descripción completa

Detalles Bibliográficos
Autores principales: Sepil, Irem, Hopkins, Ben R., Dean, Rebecca, Bath, Eleanor, Friedman, Solomon, Swanson, Ben, Ostridge, Harrison J., Harper, Lucy, Buehner, Norene A., Wolfner, Mariana F., Konietzny, Rebecca, Thézénas, Marie-Laëtitia, Sandham, Elizabeth, Charles, Philip D., Fischer, Roman, Steinhauer, Josefa, Kessler, Benedikt M., Wigby, Stuart
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7382285/
https://www.ncbi.nlm.nih.gov/pubmed/32611817
http://dx.doi.org/10.1073/pnas.2009053117
_version_ 1783563215710453760
author Sepil, Irem
Hopkins, Ben R.
Dean, Rebecca
Bath, Eleanor
Friedman, Solomon
Swanson, Ben
Ostridge, Harrison J.
Harper, Lucy
Buehner, Norene A.
Wolfner, Mariana F.
Konietzny, Rebecca
Thézénas, Marie-Laëtitia
Sandham, Elizabeth
Charles, Philip D.
Fischer, Roman
Steinhauer, Josefa
Kessler, Benedikt M.
Wigby, Stuart
author_facet Sepil, Irem
Hopkins, Ben R.
Dean, Rebecca
Bath, Eleanor
Friedman, Solomon
Swanson, Ben
Ostridge, Harrison J.
Harper, Lucy
Buehner, Norene A.
Wolfner, Mariana F.
Konietzny, Rebecca
Thézénas, Marie-Laëtitia
Sandham, Elizabeth
Charles, Philip D.
Fischer, Roman
Steinhauer, Josefa
Kessler, Benedikt M.
Wigby, Stuart
author_sort Sepil, Irem
collection PubMed
description Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the germline at the expense of the soma, suggesting differential impacts of aging on sperm and seminal fluid and trade-offs between them or, more broadly, between reproduction and lifespan. While harmful effects of male age on sperm are well known, we do not know how much seminal fluid deteriorates in comparison. Moreover, given the predicted trade-offs, it remains unclear whether systemic lifespan-extending interventions could ameliorate the declining performance of the ejaculate as a whole. Here, we address these problems using Drosophila melanogaster. We demonstrate that seminal fluid deterioration contributes to male reproductive decline via mating-dependent mechanisms that include posttranslational modifications to seminal proteins and altered seminal proteome composition and transfer. Additionally, we find that sperm production declines chronologically with age, invariant to mating activity such that older multiply mated males become infertile principally via reduced sperm transfer and viability. Our data, therefore, support the idea that both germline and soma components of the ejaculate contribute to male reproductive aging but reveal a mismatch in their aging patterns. Our data do not generally support the idea that the germline is prioritized over soma, at least, within the ejaculate. Moreover, we find that lifespan-extending systemic down-regulation of insulin signaling results in improved late-life ejaculate performance, indicating simultaneous amelioration of both somatic and reproductive aging.
format Online
Article
Text
id pubmed-7382285
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-73822852020-07-30 Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila Sepil, Irem Hopkins, Ben R. Dean, Rebecca Bath, Eleanor Friedman, Solomon Swanson, Ben Ostridge, Harrison J. Harper, Lucy Buehner, Norene A. Wolfner, Mariana F. Konietzny, Rebecca Thézénas, Marie-Laëtitia Sandham, Elizabeth Charles, Philip D. Fischer, Roman Steinhauer, Josefa Kessler, Benedikt M. Wigby, Stuart Proc Natl Acad Sci U S A Biological Sciences Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the germline at the expense of the soma, suggesting differential impacts of aging on sperm and seminal fluid and trade-offs between them or, more broadly, between reproduction and lifespan. While harmful effects of male age on sperm are well known, we do not know how much seminal fluid deteriorates in comparison. Moreover, given the predicted trade-offs, it remains unclear whether systemic lifespan-extending interventions could ameliorate the declining performance of the ejaculate as a whole. Here, we address these problems using Drosophila melanogaster. We demonstrate that seminal fluid deterioration contributes to male reproductive decline via mating-dependent mechanisms that include posttranslational modifications to seminal proteins and altered seminal proteome composition and transfer. Additionally, we find that sperm production declines chronologically with age, invariant to mating activity such that older multiply mated males become infertile principally via reduced sperm transfer and viability. Our data, therefore, support the idea that both germline and soma components of the ejaculate contribute to male reproductive aging but reveal a mismatch in their aging patterns. Our data do not generally support the idea that the germline is prioritized over soma, at least, within the ejaculate. Moreover, we find that lifespan-extending systemic down-regulation of insulin signaling results in improved late-life ejaculate performance, indicating simultaneous amelioration of both somatic and reproductive aging. National Academy of Sciences 2020-07-21 2020-07-01 /pmc/articles/PMC7382285/ /pubmed/32611817 http://dx.doi.org/10.1073/pnas.2009053117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Sepil, Irem
Hopkins, Ben R.
Dean, Rebecca
Bath, Eleanor
Friedman, Solomon
Swanson, Ben
Ostridge, Harrison J.
Harper, Lucy
Buehner, Norene A.
Wolfner, Mariana F.
Konietzny, Rebecca
Thézénas, Marie-Laëtitia
Sandham, Elizabeth
Charles, Philip D.
Fischer, Roman
Steinhauer, Josefa
Kessler, Benedikt M.
Wigby, Stuart
Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title_full Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title_fullStr Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title_full_unstemmed Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title_short Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila
title_sort male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in drosophila
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7382285/
https://www.ncbi.nlm.nih.gov/pubmed/32611817
http://dx.doi.org/10.1073/pnas.2009053117
work_keys_str_mv AT sepilirem malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT hopkinsbenr malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT deanrebecca malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT batheleanor malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT friedmansolomon malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT swansonben malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT ostridgeharrisonj malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT harperlucy malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT buehnernorenea malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT wolfnermarianaf malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT konietznyrebecca malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT thezenasmarielaetitia malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT sandhamelizabeth malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT charlesphilipd malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT fischerroman malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT steinhauerjosefa malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT kesslerbenediktm malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila
AT wigbystuart malereproductiveagingarisesviamultifacetedmatingdependentspermandseminalproteomedeclinesbutispostponableindrosophila