Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans

Organisms are exposed to temperatures that vary, for example on diurnal and seasonal time scales. Thus, the ability to behaviorally and/or physiologically respond to variation in temperatures is a fundamental requirement for long-term persistence. Studies on thermal biology in ectotherms are typical...

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Main Authors: Jesper G. Sørensen, Tommaso Manenti, Jesper S. Bechsgaard, Mads F. Schou, Torsten N. Kristensen, Volker Loeschcke
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2020.555843/full
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author Jesper G. Sørensen
Tommaso Manenti
Jesper S. Bechsgaard
Mads F. Schou
Torsten N. Kristensen
Volker Loeschcke
author_facet Jesper G. Sørensen
Tommaso Manenti
Jesper S. Bechsgaard
Mads F. Schou
Torsten N. Kristensen
Volker Loeschcke
author_sort Jesper G. Sørensen
collection DOAJ
description Organisms are exposed to temperatures that vary, for example on diurnal and seasonal time scales. Thus, the ability to behaviorally and/or physiologically respond to variation in temperatures is a fundamental requirement for long-term persistence. Studies on thermal biology in ectotherms are typically performed under constant laboratory conditions, which differ markedly from the variation in temperature across time and space in nature. Here, we investigate evolutionary adaptation and environmentally induced plastic responses of Drosophila simulans to no fluctuations (constant), predictable fluctuations or unpredictable fluctuations in temperature. We whole-genome sequenced populations exposed to 20 generations of experimental evolution under the three thermal regimes and examined the proteome after short-term exposure to the same three regimes. We find that unpredictable fluctuations cause the strongest response at both genome and proteome levels. The loci showing evolutionary responses were generally unique to each thermal regime, but a minor overlap suggests either common laboratory adaptation or that some loci were involved in the adaptation to multiple thermal regimes. The evolutionary response, i.e., loci under selection, did not coincide with induced responses of the proteome. Thus, genes under selection in fluctuating thermal environments are distinct from genes important for the adaptive plastic response observed within a generation. This information is key to obtain a better understanding and prediction of the effects of future increases in both mean and variability of temperatures.
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spelling doaj.art-aff0ce2f3e4043e6afeb20d65cac95122022-12-21T23:51:53ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-10-011110.3389/fgene.2020.555843555843Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulansJesper G. Sørensen0Tommaso Manenti1Jesper S. Bechsgaard2Mads F. Schou3Torsten N. Kristensen4Volker Loeschcke5Department of Biology, Aarhus University, Aarhus, DenmarkDepartment of Biology, Aarhus University, Aarhus, DenmarkDepartment of Biology, Aarhus University, Aarhus, DenmarkDepartment of Biology, Lund University, Lund, SwedenDepartment of Chemistry and Bioscience, Aalborg University, Aalborg, DenmarkDepartment of Biology, Aarhus University, Aarhus, DenmarkOrganisms are exposed to temperatures that vary, for example on diurnal and seasonal time scales. Thus, the ability to behaviorally and/or physiologically respond to variation in temperatures is a fundamental requirement for long-term persistence. Studies on thermal biology in ectotherms are typically performed under constant laboratory conditions, which differ markedly from the variation in temperature across time and space in nature. Here, we investigate evolutionary adaptation and environmentally induced plastic responses of Drosophila simulans to no fluctuations (constant), predictable fluctuations or unpredictable fluctuations in temperature. We whole-genome sequenced populations exposed to 20 generations of experimental evolution under the three thermal regimes and examined the proteome after short-term exposure to the same three regimes. We find that unpredictable fluctuations cause the strongest response at both genome and proteome levels. The loci showing evolutionary responses were generally unique to each thermal regime, but a minor overlap suggests either common laboratory adaptation or that some loci were involved in the adaptation to multiple thermal regimes. The evolutionary response, i.e., loci under selection, did not coincide with induced responses of the proteome. Thus, genes under selection in fluctuating thermal environments are distinct from genes important for the adaptive plastic response observed within a generation. This information is key to obtain a better understanding and prediction of the effects of future increases in both mean and variability of temperatures.https://www.frontiersin.org/articles/10.3389/fgene.2020.555843/fullheat tolerancegenomicsproteomicsthermal fluctuationsDrosophila simulans
spellingShingle Jesper G. Sørensen
Tommaso Manenti
Jesper S. Bechsgaard
Mads F. Schou
Torsten N. Kristensen
Volker Loeschcke
Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
Frontiers in Genetics
heat tolerance
genomics
proteomics
thermal fluctuations
Drosophila simulans
title Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
title_full Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
title_fullStr Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
title_full_unstemmed Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
title_short Pronounced Plastic and Evolutionary Responses to Unpredictable Thermal Fluctuations in Drosophila simulans
title_sort pronounced plastic and evolutionary responses to unpredictable thermal fluctuations in drosophila simulans
topic heat tolerance
genomics
proteomics
thermal fluctuations
Drosophila simulans
url https://www.frontiersin.org/articles/10.3389/fgene.2020.555843/full
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