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Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis

BACKGROUND: Life-history theory predicts a trade-off between investment into immune defence and other fitness-related traits. Accordingly, individuals are expected to upregulate their immune response when subjected to immune challenge. However, this is predicted to come at the expense of investment...

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Autores principales: Nystrand, M., Dowling, D. K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7541220/
https://www.ncbi.nlm.nih.gov/pubmed/33028304
http://dx.doi.org/10.1186/s12915-020-00856-7
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author Nystrand, M.
Dowling, D. K.
author_facet Nystrand, M.
Dowling, D. K.
author_sort Nystrand, M.
collection PubMed
description BACKGROUND: Life-history theory predicts a trade-off between investment into immune defence and other fitness-related traits. Accordingly, individuals are expected to upregulate their immune response when subjected to immune challenge. However, this is predicted to come at the expense of investment into a range of other traits that are costly to maintain, such as growth, reproduction and survival. Currently, it remains unclear whether the magnitude of such costs, and trade-offs involving immune investment and other traits, manifests consistently across species and sexes. To address this, we conducted a meta-analysis to investigate how changes in sex, ontogenetic stage and environmental factors shape phenotypic trait expression following an immune challenge. RESULTS: We explored the effects of immune challenge on three types of traits across sexually reproducing metazoans: life-history, morphological and proximate immune traits (235 effect sizes, 53 studies, 37 species [21 invertebrates vs. 16 vertebrates]). We report a general negative effect of immune challenge on survival and reproduction, a positive effect on immune trait expression, but no effect on morphology or development time. The negative effects of immune challenge on reproductive traits and survival were larger in females than males. We also report a pronounced effect of the immune treatment agent used (e.g. whether the treatment involved a live pathogen or not) on the host response to immune challenge, and find an effect of mating status on the host response in invertebrates. CONCLUSION: These results suggest that costs associated with immune deployment following an immune challenge are context-dependent and differ consistently in their magnitude across the sexes of diverse taxonomic lineages. We synthesise and discuss the outcomes in the context of evolutionary theory on sex differences in life-history and highlight the need for future studies to carefully consider the design of experiments aimed at disentangling the costs of immune deployment.
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spelling pubmed-75412202020-10-08 Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis Nystrand, M. Dowling, D. K. BMC Biol Research Article BACKGROUND: Life-history theory predicts a trade-off between investment into immune defence and other fitness-related traits. Accordingly, individuals are expected to upregulate their immune response when subjected to immune challenge. However, this is predicted to come at the expense of investment into a range of other traits that are costly to maintain, such as growth, reproduction and survival. Currently, it remains unclear whether the magnitude of such costs, and trade-offs involving immune investment and other traits, manifests consistently across species and sexes. To address this, we conducted a meta-analysis to investigate how changes in sex, ontogenetic stage and environmental factors shape phenotypic trait expression following an immune challenge. RESULTS: We explored the effects of immune challenge on three types of traits across sexually reproducing metazoans: life-history, morphological and proximate immune traits (235 effect sizes, 53 studies, 37 species [21 invertebrates vs. 16 vertebrates]). We report a general negative effect of immune challenge on survival and reproduction, a positive effect on immune trait expression, but no effect on morphology or development time. The negative effects of immune challenge on reproductive traits and survival were larger in females than males. We also report a pronounced effect of the immune treatment agent used (e.g. whether the treatment involved a live pathogen or not) on the host response to immune challenge, and find an effect of mating status on the host response in invertebrates. CONCLUSION: These results suggest that costs associated with immune deployment following an immune challenge are context-dependent and differ consistently in their magnitude across the sexes of diverse taxonomic lineages. We synthesise and discuss the outcomes in the context of evolutionary theory on sex differences in life-history and highlight the need for future studies to carefully consider the design of experiments aimed at disentangling the costs of immune deployment. BioMed Central 2020-10-07 /pmc/articles/PMC7541220/ /pubmed/33028304 http://dx.doi.org/10.1186/s12915-020-00856-7 Text en © The Author(s) 2020 Open AccessThis 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/. 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 in a credit line to the data.
spellingShingle Research Article
Nystrand, M.
Dowling, D. K.
Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title_full Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title_fullStr Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title_full_unstemmed Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title_short Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
title_sort effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans—a meta-analysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7541220/
https://www.ncbi.nlm.nih.gov/pubmed/33028304
http://dx.doi.org/10.1186/s12915-020-00856-7
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