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Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex

Invasive species must often survive combinations of environmental conditions that differ considerably from their native range; however, for a given species it is unclear whether improved tolerance is the result of phenotypic plasticity or genetic adaptation (or both). Agrilus planipennis (Coleoptera...

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Autores principales: Duell, Meghan E., Gray, Meghan T., Roe, Amanda D., MacQuarrie, Chris J.K., Sinclair, Brent J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387492/
https://www.ncbi.nlm.nih.gov/pubmed/36003259
http://dx.doi.org/10.1016/j.cris.2022.100031
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author Duell, Meghan E.
Gray, Meghan T.
Roe, Amanda D.
MacQuarrie, Chris J.K.
Sinclair, Brent J.
author_facet Duell, Meghan E.
Gray, Meghan T.
Roe, Amanda D.
MacQuarrie, Chris J.K.
Sinclair, Brent J.
author_sort Duell, Meghan E.
collection PubMed
description Invasive species must often survive combinations of environmental conditions that differ considerably from their native range; however, for a given species it is unclear whether improved tolerance is the result of phenotypic plasticity or genetic adaptation (or both). Agrilus planipennis (Coleoptera: Buprestidae; the emerald ash borer) is an invasive pest of Fraxinus trees in North America and Europe. Previous studies in SW Ontario, Canada, showed that A. planipennis is freeze avoidant, preventing internal ice formation by accumulating Molar concentrations of glycerol in its hemolymph and depressing its supercooling point (SCP, the temperature at which it freezes). The cold tolerance of these SW Ontario animals was used to predict potential distribution, revealing that some Canadian cities should be too cold to allow populations to persist. However, a small population of A. planipennis has persisted in Winnipeg, Manitoba, Canada, through several severe ‘polar vortex’ events. In 2018/19, we collected A. planipennis larvae and prepupae from Winnipeg, MB and Southern Ontario, and found that individuals from Winnipeg were extremely cold tolerant – with SCPs as low as -52°C in prepupae (compared to -32°C in SW Ontario), and observed survival of unfrozen individuals exposed to -50°C for one hour. This cold tolerance was accompanied by higher hemolymph osmolality and glycerol concentration than in the SW Ontario individuals. To distinguish between phenotypic plasticity and local adaptation, in 2020/21 we overwintered Winnipeg-sourced individuals either outdoors in SW Ontario or in a simulated Winnipeg winter. Simulated Winnipeg winter individuals had cold tolerance similar to those overwintered in Winnipeg, while SW Ontario overwintered individuals had cold tolerance similar to those collected previously in the region. The simulated winter individuals had higher hemolymph glycerol concentrations than SW Ontario overwintered animals, at least in part due to greater dehydration. Thus, A. planipennis are cold-tolerant enough to survive some of the harshest winters where their host trees can grow, and most likely attain this cold tolerance via phenotypic plasticity. These findings raise the importance of delineating sensitivity of conclusions to unexpected phenotypic plasticity when predicting potential distributions of new invasives or responses to climate change.
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spelling pubmed-93874922022-08-23 Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex Duell, Meghan E. Gray, Meghan T. Roe, Amanda D. MacQuarrie, Chris J.K. Sinclair, Brent J. Curr Res Insect Sci Research Article Invasive species must often survive combinations of environmental conditions that differ considerably from their native range; however, for a given species it is unclear whether improved tolerance is the result of phenotypic plasticity or genetic adaptation (or both). Agrilus planipennis (Coleoptera: Buprestidae; the emerald ash borer) is an invasive pest of Fraxinus trees in North America and Europe. Previous studies in SW Ontario, Canada, showed that A. planipennis is freeze avoidant, preventing internal ice formation by accumulating Molar concentrations of glycerol in its hemolymph and depressing its supercooling point (SCP, the temperature at which it freezes). The cold tolerance of these SW Ontario animals was used to predict potential distribution, revealing that some Canadian cities should be too cold to allow populations to persist. However, a small population of A. planipennis has persisted in Winnipeg, Manitoba, Canada, through several severe ‘polar vortex’ events. In 2018/19, we collected A. planipennis larvae and prepupae from Winnipeg, MB and Southern Ontario, and found that individuals from Winnipeg were extremely cold tolerant – with SCPs as low as -52°C in prepupae (compared to -32°C in SW Ontario), and observed survival of unfrozen individuals exposed to -50°C for one hour. This cold tolerance was accompanied by higher hemolymph osmolality and glycerol concentration than in the SW Ontario individuals. To distinguish between phenotypic plasticity and local adaptation, in 2020/21 we overwintered Winnipeg-sourced individuals either outdoors in SW Ontario or in a simulated Winnipeg winter. Simulated Winnipeg winter individuals had cold tolerance similar to those overwintered in Winnipeg, while SW Ontario overwintered individuals had cold tolerance similar to those collected previously in the region. The simulated winter individuals had higher hemolymph glycerol concentrations than SW Ontario overwintered animals, at least in part due to greater dehydration. Thus, A. planipennis are cold-tolerant enough to survive some of the harshest winters where their host trees can grow, and most likely attain this cold tolerance via phenotypic plasticity. These findings raise the importance of delineating sensitivity of conclusions to unexpected phenotypic plasticity when predicting potential distributions of new invasives or responses to climate change. Elsevier 2022-02-03 /pmc/articles/PMC9387492/ /pubmed/36003259 http://dx.doi.org/10.1016/j.cris.2022.100031 Text en Crown Copyright © 2022 Published by Elsevier B.V. https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Research Article
Duell, Meghan E.
Gray, Meghan T.
Roe, Amanda D.
MacQuarrie, Chris J.K.
Sinclair, Brent J.
Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title_full Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title_fullStr Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title_full_unstemmed Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title_short Plasticity drives extreme cold tolerance of emerald ash borer (Agrilus planipennis) during a polar vortex
title_sort plasticity drives extreme cold tolerance of emerald ash borer (agrilus planipennis) during a polar vortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387492/
https://www.ncbi.nlm.nih.gov/pubmed/36003259
http://dx.doi.org/10.1016/j.cris.2022.100031
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