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Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster

Environmental stresses such as extreme temperatures, dehydration and food deprivation may have distinct consequences for different age-classes and for males and females across species. Here we investigate a natural population of the model organism Drosophila melanogaster. Males and females at ages 3...

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Autores principales: Kristensen, Torsten Nygaard, Loeschcke, Volker, Tan, Qihua, Pertoldi, Cino, Mengel-From, Jonas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6707197/
https://www.ncbi.nlm.nih.gov/pubmed/31444377
http://dx.doi.org/10.1038/s41598-019-48752-7
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author Kristensen, Torsten Nygaard
Loeschcke, Volker
Tan, Qihua
Pertoldi, Cino
Mengel-From, Jonas
author_facet Kristensen, Torsten Nygaard
Loeschcke, Volker
Tan, Qihua
Pertoldi, Cino
Mengel-From, Jonas
author_sort Kristensen, Torsten Nygaard
collection PubMed
description Environmental stresses such as extreme temperatures, dehydration and food deprivation may have distinct consequences for different age-classes and for males and females across species. Here we investigate a natural population of the model organism Drosophila melanogaster. Males and females at ages 3, 19 and 35 days were tested for stress resistance; i.e. the ability of flies to cope with starvation and both cold and hot temperatures. Further, we tested a measure of metabolic efficiency, namely mitochondrial DNA copy number (mtDNA CN) in both sexes at all three age-classes. We hypothesize that stress resistance is reduced at old age and more so in males, and that mtDNA CN is a biomarker for sex- and age-dependent reductions in the ability to cope with harsh environments. We show that: (1) males exhibit reduced starvation tolerance at old age, whereas older females are better in coping with periods without food compared to younger females, (2) heat tolerance decreases with increasing age in males but not in females, (3) cold tolerance is reduced at old age in both sexes, and (4) old males have reduced mtDNA CN whereas mtDNA CN slightly increases with age in females. In conclusion, our data provide strong evidence for trait and sex specific consequences of aging with females generally being better at coping with environmental stress at old age. The reduced mtDNA CN in old males suggests reduced metabolic efficiency and this may partly explain why males are less stress tolerant at old age than females. We suggest that mtDNA CN might be a suitable biomarker for physiological robustness. Our findings likely extend to other taxa than Drosophila and therefore we discuss the observations in relation to aging and sex specific lifespan across species.
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spelling pubmed-67071972019-09-08 Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster Kristensen, Torsten Nygaard Loeschcke, Volker Tan, Qihua Pertoldi, Cino Mengel-From, Jonas Sci Rep Article Environmental stresses such as extreme temperatures, dehydration and food deprivation may have distinct consequences for different age-classes and for males and females across species. Here we investigate a natural population of the model organism Drosophila melanogaster. Males and females at ages 3, 19 and 35 days were tested for stress resistance; i.e. the ability of flies to cope with starvation and both cold and hot temperatures. Further, we tested a measure of metabolic efficiency, namely mitochondrial DNA copy number (mtDNA CN) in both sexes at all three age-classes. We hypothesize that stress resistance is reduced at old age and more so in males, and that mtDNA CN is a biomarker for sex- and age-dependent reductions in the ability to cope with harsh environments. We show that: (1) males exhibit reduced starvation tolerance at old age, whereas older females are better in coping with periods without food compared to younger females, (2) heat tolerance decreases with increasing age in males but not in females, (3) cold tolerance is reduced at old age in both sexes, and (4) old males have reduced mtDNA CN whereas mtDNA CN slightly increases with age in females. In conclusion, our data provide strong evidence for trait and sex specific consequences of aging with females generally being better at coping with environmental stress at old age. The reduced mtDNA CN in old males suggests reduced metabolic efficiency and this may partly explain why males are less stress tolerant at old age than females. We suggest that mtDNA CN might be a suitable biomarker for physiological robustness. Our findings likely extend to other taxa than Drosophila and therefore we discuss the observations in relation to aging and sex specific lifespan across species. Nature Publishing Group UK 2019-08-23 /pmc/articles/PMC6707197/ /pubmed/31444377 http://dx.doi.org/10.1038/s41598-019-48752-7 Text en © The Author(s) 2019 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/.
spellingShingle Article
Kristensen, Torsten Nygaard
Loeschcke, Volker
Tan, Qihua
Pertoldi, Cino
Mengel-From, Jonas
Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title_full Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title_fullStr Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title_full_unstemmed Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title_short Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster
title_sort sex and age specific reduction in stress resistance and mitochondrial dna copy number in drosophila melanogaster
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6707197/
https://www.ncbi.nlm.nih.gov/pubmed/31444377
http://dx.doi.org/10.1038/s41598-019-48752-7
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