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Social isolation shortens lifespan through oxidative stress in ants

Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, w...

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Autores principales: Koto, Akiko, Tamura, Makoto, Wong, Pui Shan, Aburatani, Sachiyo, Privman, Eyal, Stoffel, Céline, Crespi, Alessandro, McKenzie, Sean Keane, La Mendola, Christine, Kay, Tomas, Keller, Laurent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533837/
https://www.ncbi.nlm.nih.gov/pubmed/37758727
http://dx.doi.org/10.1038/s41467-023-41140-w
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author Koto, Akiko
Tamura, Makoto
Wong, Pui Shan
Aburatani, Sachiyo
Privman, Eyal
Stoffel, Céline
Crespi, Alessandro
McKenzie, Sean Keane
La Mendola, Christine
Kay, Tomas
Keller, Laurent
author_facet Koto, Akiko
Tamura, Makoto
Wong, Pui Shan
Aburatani, Sachiyo
Privman, Eyal
Stoffel, Céline
Crespi, Alessandro
McKenzie, Sean Keane
La Mendola, Christine
Kay, Tomas
Keller, Laurent
author_sort Koto, Akiko
collection PubMed
description Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, we show that social isolation induces hyperactivity, alters space-use, and reduces lifespan via changes in the expression of genes with key roles in oxidation-reduction and an associated accumulation of reactive oxygen species. These physiological effects are localized to the fat body and oenocytes, which perform liver-like functions in insects. We use pharmacological manipulations to demonstrate that the oxidation-reduction pathway causally underpins the detrimental effects of social isolation on behavior and lifespan. These findings have important implications for our understanding of how social isolation affects behavior and lifespan in general.
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spelling pubmed-105338372023-09-29 Social isolation shortens lifespan through oxidative stress in ants Koto, Akiko Tamura, Makoto Wong, Pui Shan Aburatani, Sachiyo Privman, Eyal Stoffel, Céline Crespi, Alessandro McKenzie, Sean Keane La Mendola, Christine Kay, Tomas Keller, Laurent Nat Commun Article Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, we show that social isolation induces hyperactivity, alters space-use, and reduces lifespan via changes in the expression of genes with key roles in oxidation-reduction and an associated accumulation of reactive oxygen species. These physiological effects are localized to the fat body and oenocytes, which perform liver-like functions in insects. We use pharmacological manipulations to demonstrate that the oxidation-reduction pathway causally underpins the detrimental effects of social isolation on behavior and lifespan. These findings have important implications for our understanding of how social isolation affects behavior and lifespan in general. Nature Publishing Group UK 2023-09-27 /pmc/articles/PMC10533837/ /pubmed/37758727 http://dx.doi.org/10.1038/s41467-023-41140-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Koto, Akiko
Tamura, Makoto
Wong, Pui Shan
Aburatani, Sachiyo
Privman, Eyal
Stoffel, Céline
Crespi, Alessandro
McKenzie, Sean Keane
La Mendola, Christine
Kay, Tomas
Keller, Laurent
Social isolation shortens lifespan through oxidative stress in ants
title Social isolation shortens lifespan through oxidative stress in ants
title_full Social isolation shortens lifespan through oxidative stress in ants
title_fullStr Social isolation shortens lifespan through oxidative stress in ants
title_full_unstemmed Social isolation shortens lifespan through oxidative stress in ants
title_short Social isolation shortens lifespan through oxidative stress in ants
title_sort social isolation shortens lifespan through oxidative stress in ants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533837/
https://www.ncbi.nlm.nih.gov/pubmed/37758727
http://dx.doi.org/10.1038/s41467-023-41140-w
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