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Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system

Climate change has profound effects on infectious disease dynamics, yet the impacts of increased short-term temperature fluctuations on disease spread remain poorly understood. We empirically tested the theoretical prediction that short-term thermal fluctuations suppress endemic infection prevalence...

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Autores principales: Krichel, Leila, Kirk, Devin, Pencer, Clara, Hönig, Madison, Wadhawan, Kiran, Krkošek, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491407/
https://www.ncbi.nlm.nih.gov/pubmed/37683040
http://dx.doi.org/10.1371/journal.pbio.3002260
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author Krichel, Leila
Kirk, Devin
Pencer, Clara
Hönig, Madison
Wadhawan, Kiran
Krkošek, Martin
author_facet Krichel, Leila
Kirk, Devin
Pencer, Clara
Hönig, Madison
Wadhawan, Kiran
Krkošek, Martin
author_sort Krichel, Leila
collection PubMed
description Climate change has profound effects on infectious disease dynamics, yet the impacts of increased short-term temperature fluctuations on disease spread remain poorly understood. We empirically tested the theoretical prediction that short-term thermal fluctuations suppress endemic infection prevalence at the pathogen’s thermal optimum. This prediction follows from a mechanistic disease transmission model analyzed using stochastic simulations of the model parameterized with thermal performance curves (TPCs) from metabolic scaling theory and using nonlinear averaging, which predicts ecological outcomes consistent with Jensen’s inequality (i.e., reduced performance around concave-down portions of a thermal response curve). Experimental observations of replicated epidemics of the microparasite Ordospora colligata in Daphnia magna populations indicate that temperature variability had the opposite effect of our theoretical predictions and instead increase endemic infection prevalence. This positive effect of temperature variability is qualitatively consistent with a published hypothesis that parasites may acclimate more rapidly to fluctuating temperatures than their hosts; however, incorporating hypothetical effects of delayed host acclimation into the mechanistic transmission model did not fully account for the observed pattern. The experimental data indicate that shifts in the distribution of infection burden underlie the positive effect of temperature fluctuations on endemic prevalence. The increase in disease risk associated with climate fluctuations may therefore result from disease processes interacting across scales, particularly within-host dynamics, that are not captured by combining standard transmission models with metabolic scaling theory.
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spelling pubmed-104914072023-09-09 Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system Krichel, Leila Kirk, Devin Pencer, Clara Hönig, Madison Wadhawan, Kiran Krkošek, Martin PLoS Biol Research Article Climate change has profound effects on infectious disease dynamics, yet the impacts of increased short-term temperature fluctuations on disease spread remain poorly understood. We empirically tested the theoretical prediction that short-term thermal fluctuations suppress endemic infection prevalence at the pathogen’s thermal optimum. This prediction follows from a mechanistic disease transmission model analyzed using stochastic simulations of the model parameterized with thermal performance curves (TPCs) from metabolic scaling theory and using nonlinear averaging, which predicts ecological outcomes consistent with Jensen’s inequality (i.e., reduced performance around concave-down portions of a thermal response curve). Experimental observations of replicated epidemics of the microparasite Ordospora colligata in Daphnia magna populations indicate that temperature variability had the opposite effect of our theoretical predictions and instead increase endemic infection prevalence. This positive effect of temperature variability is qualitatively consistent with a published hypothesis that parasites may acclimate more rapidly to fluctuating temperatures than their hosts; however, incorporating hypothetical effects of delayed host acclimation into the mechanistic transmission model did not fully account for the observed pattern. The experimental data indicate that shifts in the distribution of infection burden underlie the positive effect of temperature fluctuations on endemic prevalence. The increase in disease risk associated with climate fluctuations may therefore result from disease processes interacting across scales, particularly within-host dynamics, that are not captured by combining standard transmission models with metabolic scaling theory. Public Library of Science 2023-09-08 /pmc/articles/PMC10491407/ /pubmed/37683040 http://dx.doi.org/10.1371/journal.pbio.3002260 Text en © 2023 Krichel et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Krichel, Leila
Kirk, Devin
Pencer, Clara
Hönig, Madison
Wadhawan, Kiran
Krkošek, Martin
Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title_full Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title_fullStr Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title_full_unstemmed Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title_short Short-term temperature fluctuations increase disease in a Daphnia-parasite infectious disease system
title_sort short-term temperature fluctuations increase disease in a daphnia-parasite infectious disease system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491407/
https://www.ncbi.nlm.nih.gov/pubmed/37683040
http://dx.doi.org/10.1371/journal.pbio.3002260
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