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Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae

The temperature dependence of infection reflects changes in performance of parasites and hosts. High temperatures often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit endothermic thermoregulation—rare among insects—that can favor resistance to pa...

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Autores principales: Palmer-Young, Evan C., Ryabov, Eugene V., Markowitz, Lindsey M., Boncristiani, Dawn L., Grubbs, Kyle, Pawar, Asha, Peterson, Raymond, Evans, Jay D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10042853/
https://www.ncbi.nlm.nih.gov/pubmed/36973325
http://dx.doi.org/10.1038/s42003-023-04704-6
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author Palmer-Young, Evan C.
Ryabov, Eugene V.
Markowitz, Lindsey M.
Boncristiani, Dawn L.
Grubbs, Kyle
Pawar, Asha
Peterson, Raymond
Evans, Jay D.
author_facet Palmer-Young, Evan C.
Ryabov, Eugene V.
Markowitz, Lindsey M.
Boncristiani, Dawn L.
Grubbs, Kyle
Pawar, Asha
Peterson, Raymond
Evans, Jay D.
author_sort Palmer-Young, Evan C.
collection PubMed
description The temperature dependence of infection reflects changes in performance of parasites and hosts. High temperatures often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit endothermic thermoregulation—rare among insects—that can favor resistance to parasites. However, viruses are heavily host-dependent, suggesting that viral infection could be supported—not threatened—by optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape infection, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied <2-fold over a > 30 °C interval spanning temperatures typical of ectothermic insects and honey bees. In contrast, honey bee performance peaked at high (≥ 35 °C) temperatures and was highly temperature-sensitive. Although these results suggested that increasing temperature would favor hosts over viruses, the temperature dependence of pupal infection matched that of pupal development, falling only near pupae’s upper thermal limits. Our results reflect the host-dependent nature of viruses, suggesting that infection is accelerated—not curtailed—by optimum host function, contradicting predictions based on relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival that limit the viability of bee ‘fever’.
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spelling pubmed-100428532023-03-29 Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae Palmer-Young, Evan C. Ryabov, Eugene V. Markowitz, Lindsey M. Boncristiani, Dawn L. Grubbs, Kyle Pawar, Asha Peterson, Raymond Evans, Jay D. Commun Biol Article The temperature dependence of infection reflects changes in performance of parasites and hosts. High temperatures often mitigate infection by favoring heat-tolerant hosts over heat-sensitive parasites. Honey bees exhibit endothermic thermoregulation—rare among insects—that can favor resistance to parasites. However, viruses are heavily host-dependent, suggesting that viral infection could be supported—not threatened—by optimum host function. To understand how temperature-driven changes in performance of viruses and hosts shape infection, we compared the temperature dependence of isolated viral enzyme activity, three honey bee traits, and infection of honey bee pupae. Viral enzyme activity varied <2-fold over a > 30 °C interval spanning temperatures typical of ectothermic insects and honey bees. In contrast, honey bee performance peaked at high (≥ 35 °C) temperatures and was highly temperature-sensitive. Although these results suggested that increasing temperature would favor hosts over viruses, the temperature dependence of pupal infection matched that of pupal development, falling only near pupae’s upper thermal limits. Our results reflect the host-dependent nature of viruses, suggesting that infection is accelerated—not curtailed—by optimum host function, contradicting predictions based on relative performance of parasites and hosts, and suggesting tradeoffs between infection resistance and host survival that limit the viability of bee ‘fever’. Nature Publishing Group UK 2023-03-27 /pmc/articles/PMC10042853/ /pubmed/36973325 http://dx.doi.org/10.1038/s42003-023-04704-6 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 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 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Palmer-Young, Evan C.
Ryabov, Eugene V.
Markowitz, Lindsey M.
Boncristiani, Dawn L.
Grubbs, Kyle
Pawar, Asha
Peterson, Raymond
Evans, Jay D.
Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title_full Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title_fullStr Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title_full_unstemmed Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title_short Host-driven temperature dependence of Deformed wing virus infection in honey bee pupae
title_sort host-driven temperature dependence of deformed wing virus infection in honey bee pupae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10042853/
https://www.ncbi.nlm.nih.gov/pubmed/36973325
http://dx.doi.org/10.1038/s42003-023-04704-6
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