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Host sex and age influence endoparasite burdens in the gray mouse lemur

INTRODUCTION: Immunosenescence (deteriorating immune function at old age) affects humans and laboratory animals, but little is known about immunosenescence in natural populations despite its potential importance for population and disease dynamics and individual fitness. Although life histories and...

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Autores principales: Hämäläinen, Anni, Raharivololona, Brigitte, Ravoniarimbinina, Pascaline, Kraus, Cornelia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4591582/
https://www.ncbi.nlm.nih.gov/pubmed/26435728
http://dx.doi.org/10.1186/s12983-015-0118-9
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author Hämäläinen, Anni
Raharivololona, Brigitte
Ravoniarimbinina, Pascaline
Kraus, Cornelia
author_facet Hämäläinen, Anni
Raharivololona, Brigitte
Ravoniarimbinina, Pascaline
Kraus, Cornelia
author_sort Hämäläinen, Anni
collection PubMed
description INTRODUCTION: Immunosenescence (deteriorating immune function at old age) affects humans and laboratory animals, but little is known about immunosenescence in natural populations despite its potential importance for population and disease dynamics and individual fitness. Although life histories and immune system profiles often differ between the sexes, sex-specific effects of aging on health are rarely studied in the wild. Life history theory predicts that due to their shorter lifespan and higher investment into reproduction at the expense of immune defences, males might experience accelerated immunosenescence. We tested this hypothesis by examining sex-specific age trajectories of endoparasite burden (helminth prevalence and morphotype richness measured via fecal egg counts), an indicator of overall health, in wild gray mouse lemurs (Microcebus murinus). To account for potential interactions between seasonality and host sex or age we examined the predictors of parasite burdens separately for the dry and rainy season. RESULTS: Contrary to the prediction of immunosenescence, parasite prevalence and morphotype richness decreased at old age in the dry season, indicating acquired immunity by older animals. This pattern was primarily caused by within-individual decline in parasite loads rather than the earlier mortality of highly parasitized individuals. With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance. Besides this sex*age interaction, host age was uncorrelated with rainy season parasite loads. Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness. CONCLUSIONS: These results provide rare information about the age-related patterns of health in a wild vertebrate population and suggest improvement rather than senescence in the ability to resist helminth infections at old age. Overall, males appear not to suffer from earlier immunosenescence relative to females. This may partially reflect the earlier mortality of males, which can render senescence difficult to detect. While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-015-0118-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-45915822015-10-03 Host sex and age influence endoparasite burdens in the gray mouse lemur Hämäläinen, Anni Raharivololona, Brigitte Ravoniarimbinina, Pascaline Kraus, Cornelia Front Zool Research INTRODUCTION: Immunosenescence (deteriorating immune function at old age) affects humans and laboratory animals, but little is known about immunosenescence in natural populations despite its potential importance for population and disease dynamics and individual fitness. Although life histories and immune system profiles often differ between the sexes, sex-specific effects of aging on health are rarely studied in the wild. Life history theory predicts that due to their shorter lifespan and higher investment into reproduction at the expense of immune defences, males might experience accelerated immunosenescence. We tested this hypothesis by examining sex-specific age trajectories of endoparasite burden (helminth prevalence and morphotype richness measured via fecal egg counts), an indicator of overall health, in wild gray mouse lemurs (Microcebus murinus). To account for potential interactions between seasonality and host sex or age we examined the predictors of parasite burdens separately for the dry and rainy season. RESULTS: Contrary to the prediction of immunosenescence, parasite prevalence and morphotype richness decreased at old age in the dry season, indicating acquired immunity by older animals. This pattern was primarily caused by within-individual decline in parasite loads rather than the earlier mortality of highly parasitized individuals. With the exception of an increasing cestode prevalence in males from yearlings to prime age in the rainy season, no evidence was found of male-biased ageing in parasite resistance. Besides this sex*age interaction, host age was uncorrelated with rainy season parasite loads. Seasonality did not affect the overall parasite loads but seasonal patterns were found in the predictors of parasite prevalence and morphotype richness. CONCLUSIONS: These results provide rare information about the age-related patterns of health in a wild vertebrate population and suggest improvement rather than senescence in the ability to resist helminth infections at old age. Overall, males appear not to suffer from earlier immunosenescence relative to females. This may partially reflect the earlier mortality of males, which can render senescence difficult to detect. While helminth infections are not strongly associated with survival in wild gray mouse lemurs, parasite load may, however, reflect overall good phenotypic quality of long-lived individuals, and is a potential correlate of fitness. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12983-015-0118-9) contains supplementary material, which is available to authorized users. BioMed Central 2015-10-01 /pmc/articles/PMC4591582/ /pubmed/26435728 http://dx.doi.org/10.1186/s12983-015-0118-9 Text en © Hämäläinen et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Hämäläinen, Anni
Raharivololona, Brigitte
Ravoniarimbinina, Pascaline
Kraus, Cornelia
Host sex and age influence endoparasite burdens in the gray mouse lemur
title Host sex and age influence endoparasite burdens in the gray mouse lemur
title_full Host sex and age influence endoparasite burdens in the gray mouse lemur
title_fullStr Host sex and age influence endoparasite burdens in the gray mouse lemur
title_full_unstemmed Host sex and age influence endoparasite burdens in the gray mouse lemur
title_short Host sex and age influence endoparasite burdens in the gray mouse lemur
title_sort host sex and age influence endoparasite burdens in the gray mouse lemur
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4591582/
https://www.ncbi.nlm.nih.gov/pubmed/26435728
http://dx.doi.org/10.1186/s12983-015-0118-9
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