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Both age and social environment shape the phenotype of ant workers

Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly...

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Autores principales: Quque, Martin, Brun, Charlotte, Villette, Claire, Sueur, Cédric, Criscuolo, François, Heintz, Dimitri, Bertile, Fabrice
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9814961/
https://www.ncbi.nlm.nih.gov/pubmed/36604491
http://dx.doi.org/10.1038/s41598-022-26515-1
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author Quque, Martin
Brun, Charlotte
Villette, Claire
Sueur, Cédric
Criscuolo, François
Heintz, Dimitri
Bertile, Fabrice
author_facet Quque, Martin
Brun, Charlotte
Villette, Claire
Sueur, Cédric
Criscuolo, François
Heintz, Dimitri
Bertile, Fabrice
author_sort Quque, Martin
collection PubMed
description Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly on age. As such, untangling the effects of social role and age on worker physiology is a key step towards understanding the coevolution of sociality and aging. We performed an experimental protocol that allowed a separate analysis of these two factors using four groups of black garden ant (Lasius niger) workers: young foragers, old foragers, young nest workers, and old nest workers. We highlighted age-related differences in the proteome and metabolome of workers that were primarily related to worker subcaste and only secondarily to age. The relative abundance of proteins and metabolites suggests an improved xenobiotic detoxification, and a fuel metabolism based more on lipid use than carbohydrate use in young ants, regardless of their social role. Regardless of age, proteins related to the digestive function were more abundant in nest workers than in foragers. Old foragers were mostly characterized by weak abundances of molecules with an antibiotic activity or involved in chemical communication. Finally, our results suggest that even in tiny insects, extended lifespan may require to mitigate cancer risks. This is consistent with results found in eusocial rodents and thus opens up the discussion of shared mechanisms among distant taxa and the influence of sociality on life history traits such as longevity.
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spelling pubmed-98149612023-01-06 Both age and social environment shape the phenotype of ant workers Quque, Martin Brun, Charlotte Villette, Claire Sueur, Cédric Criscuolo, François Heintz, Dimitri Bertile, Fabrice Sci Rep Article Position within the social group has consequences on individual lifespans in diverse taxa. This is especially obvious in eusocial insects, where workers differ in both the tasks they perform and their aging rates. However, in eusocial wasps, bees and ants, the performed task usually depends strongly on age. As such, untangling the effects of social role and age on worker physiology is a key step towards understanding the coevolution of sociality and aging. We performed an experimental protocol that allowed a separate analysis of these two factors using four groups of black garden ant (Lasius niger) workers: young foragers, old foragers, young nest workers, and old nest workers. We highlighted age-related differences in the proteome and metabolome of workers that were primarily related to worker subcaste and only secondarily to age. The relative abundance of proteins and metabolites suggests an improved xenobiotic detoxification, and a fuel metabolism based more on lipid use than carbohydrate use in young ants, regardless of their social role. Regardless of age, proteins related to the digestive function were more abundant in nest workers than in foragers. Old foragers were mostly characterized by weak abundances of molecules with an antibiotic activity or involved in chemical communication. Finally, our results suggest that even in tiny insects, extended lifespan may require to mitigate cancer risks. This is consistent with results found in eusocial rodents and thus opens up the discussion of shared mechanisms among distant taxa and the influence of sociality on life history traits such as longevity. Nature Publishing Group UK 2023-01-05 /pmc/articles/PMC9814961/ /pubmed/36604491 http://dx.doi.org/10.1038/s41598-022-26515-1 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Quque, Martin
Brun, Charlotte
Villette, Claire
Sueur, Cédric
Criscuolo, François
Heintz, Dimitri
Bertile, Fabrice
Both age and social environment shape the phenotype of ant workers
title Both age and social environment shape the phenotype of ant workers
title_full Both age and social environment shape the phenotype of ant workers
title_fullStr Both age and social environment shape the phenotype of ant workers
title_full_unstemmed Both age and social environment shape the phenotype of ant workers
title_short Both age and social environment shape the phenotype of ant workers
title_sort both age and social environment shape the phenotype of ant workers
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9814961/
https://www.ncbi.nlm.nih.gov/pubmed/36604491
http://dx.doi.org/10.1038/s41598-022-26515-1
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