Thermal fluctuations affect the transcriptome through mechanisms independent of average temperature
(2016) In Scientific Reports 6(August). p.30975-30975- Abstract
- Terrestrial ectotherms are challenged by variation in both mean and variance of temperature. Phenotypic plasticity (thermal acclimation) might mitigate adverse effects, however, we lack a fundamental understanding of the molecular mechanisms of thermal acclimation and how they are affected by fluctuating temperature. Here we investigated the effect of thermal acclimation in Drosophila melanogaster on critical thermal maxima (CTmax) and associated global gene expression profiles as induced by two constant and two ecologically relevant (non-stressful) diurnally fluctuating temperature regimes. Both mean and fluctuation of temperature contributed to thermal acclimation and affected the transcriptome. The transcriptomic response to mean... (More)
- Terrestrial ectotherms are challenged by variation in both mean and variance of temperature. Phenotypic plasticity (thermal acclimation) might mitigate adverse effects, however, we lack a fundamental understanding of the molecular mechanisms of thermal acclimation and how they are affected by fluctuating temperature. Here we investigated the effect of thermal acclimation in Drosophila melanogaster on critical thermal maxima (CTmax) and associated global gene expression profiles as induced by two constant and two ecologically relevant (non-stressful) diurnally fluctuating temperature regimes. Both mean and fluctuation of temperature contributed to thermal acclimation and affected the transcriptome. The transcriptomic response to mean temperatures comprised modification of a major part of the transcriptome, while the response to fluctuations affected a much smaller set of genes, which was highly independent of both the response to a change in mean temperature and to the classic heat shock response. Although the independent transcriptional effects caused by fluctuations were relatively small, they are likely to contribute to our understanding of thermal adaptation. We provide evidence that environmental sensing, particularly phototransduction, is a central mechanism underlying the regulation of thermal acclimation to fluctuating temperatures. Thus, genes and pathways involved in phototransduction are likely of importance in fluctuating climates. It is widely accepted that global climate change will affect ectothermic organisms through changes in means and variances of temperatures 1 . However, exactly how organisms will be affected is less well understood 2 . It is, for example, not clear whether tropical or mid-latitude terrestrial ectotherms are most vulnerable to warming 3,4 . Recent studies points to a major impact of extreme events rather than mean temperatures on the distribution of populations 5–7 , and it has been argued that many species are likely to depend heavily on adaptive behavioral or physiological responses (acclimation) to survive variable and sometimes stressful thermal conditions 8–10 . Studying in depth if, when and how organisms respond to temperature challenges through modifications of physiology or behavior is therefore important for a better understanding of thermal adaptation in general and the effects of thermal variation specifically 11,12 . From laboratory studies of ectotherms we have obtained detailed information about costs and benefits of accli-mation at low and high temperatures 8,12 . Generally, beneficial thermal acclimation is known to affect thermal pref-erence and performance, including increasing tolerance to subsequent exposure to more stressful temperatures 8,13 . In nature terrestrial ectotherms are rarely exposed to constant thermal conditions, however, current knowledge of temperature acclimation relies primarily on studies at constant temperatures 14 . Hardening and acclimation at variable temperatures have been shown to induce increased heat tolerance 15,16 and might elicit a different stress response to subsequent temperature challenges compared to a pretreatment at constant temperatures 17–19 . Furthermore, the few studies investigating plastic responses to low and high temperatures in the field or under semi-natural conditions do not always support conclusions based on laboratory studies as costs and benefits may (Less)
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https://lup.lub.lu.se/record/9771992a-37f6-4715-97cf-94e2243b2128
- author
- Sørensen, Jesper Givskov ; Schou, Mads Fristrup LU ; Kristensen, Torsten Nygaard and Loeschcke, Volker
- publishing date
- 2016
- type
- Contribution to journal
- publication status
- published
- subject
- in
- Scientific Reports
- volume
- 6
- issue
- August
- pages
- 1 pages
- publisher
- Nature Publishing Group
- external identifiers
-
- pmid:27487917
- scopus:84982812673
- ISSN
- 2045-2322
- DOI
- 10.1038/srep30975
- language
- English
- LU publication?
- no
- id
- 9771992a-37f6-4715-97cf-94e2243b2128
- alternative location
- http://www.nature.com/articles/srep30975
- date added to LUP
- 2017-12-18 09:47:13
- date last changed
- 2022-03-24 23:03:30
@article{9771992a-37f6-4715-97cf-94e2243b2128,
abstract = {{Terrestrial ectotherms are challenged by variation in both mean and variance of temperature. Phenotypic plasticity (thermal acclimation) might mitigate adverse effects, however, we lack a fundamental understanding of the molecular mechanisms of thermal acclimation and how they are affected by fluctuating temperature. Here we investigated the effect of thermal acclimation in Drosophila melanogaster on critical thermal maxima (CTmax) and associated global gene expression profiles as induced by two constant and two ecologically relevant (non-stressful) diurnally fluctuating temperature regimes. Both mean and fluctuation of temperature contributed to thermal acclimation and affected the transcriptome. The transcriptomic response to mean temperatures comprised modification of a major part of the transcriptome, while the response to fluctuations affected a much smaller set of genes, which was highly independent of both the response to a change in mean temperature and to the classic heat shock response. Although the independent transcriptional effects caused by fluctuations were relatively small, they are likely to contribute to our understanding of thermal adaptation. We provide evidence that environmental sensing, particularly phototransduction, is a central mechanism underlying the regulation of thermal acclimation to fluctuating temperatures. Thus, genes and pathways involved in phototransduction are likely of importance in fluctuating climates. It is widely accepted that global climate change will affect ectothermic organisms through changes in means and variances of temperatures 1 . However, exactly how organisms will be affected is less well understood 2 . It is, for example, not clear whether tropical or mid-latitude terrestrial ectotherms are most vulnerable to warming 3,4 . Recent studies points to a major impact of extreme events rather than mean temperatures on the distribution of populations 5–7 , and it has been argued that many species are likely to depend heavily on adaptive behavioral or physiological responses (acclimation) to survive variable and sometimes stressful thermal conditions 8–10 . Studying in depth if, when and how organisms respond to temperature challenges through modifications of physiology or behavior is therefore important for a better understanding of thermal adaptation in general and the effects of thermal variation specifically 11,12 . From laboratory studies of ectotherms we have obtained detailed information about costs and benefits of accli-mation at low and high temperatures 8,12 . Generally, beneficial thermal acclimation is known to affect thermal pref-erence and performance, including increasing tolerance to subsequent exposure to more stressful temperatures 8,13 . In nature terrestrial ectotherms are rarely exposed to constant thermal conditions, however, current knowledge of temperature acclimation relies primarily on studies at constant temperatures 14 . Hardening and acclimation at variable temperatures have been shown to induce increased heat tolerance 15,16 and might elicit a different stress response to subsequent temperature challenges compared to a pretreatment at constant temperatures 17–19 . Furthermore, the few studies investigating plastic responses to low and high temperatures in the field or under semi-natural conditions do not always support conclusions based on laboratory studies as costs and benefits may}},
author = {{Sørensen, Jesper Givskov and Schou, Mads Fristrup and Kristensen, Torsten Nygaard and Loeschcke, Volker}},
issn = {{2045-2322}},
language = {{eng}},
number = {{August}},
pages = {{30975--30975}},
publisher = {{Nature Publishing Group}},
series = {{Scientific Reports}},
title = {{Thermal fluctuations affect the transcriptome through mechanisms independent of average temperature}},
url = {{http://dx.doi.org/10.1038/srep30975}},
doi = {{10.1038/srep30975}},
volume = {{6}},
year = {{2016}},
}