A widespread thermodynamic effect, but maintenance of biological rates through space across life's major domains

Research output: Contribution to journalArticleResearchpeer-review

Abstract

For over a century, the hypothesis of temperature compensation, the maintenance of similar biological rates in species from different thermal environments, has remained controversial. An alternative idea, that fitness is greater at higher temperatures (the thermodynamic effect), has gained increasing traction. This alternative hypothesis is also being used to understand large-scale biodiversity responses to environmental change. Yet evidence in favour of each of these contrasting hypotheses continues to emerge. In consequence, the fundamental nature of organismal thermal responses and its implications remain unresolved. Here, we investigate these ideas explicitly using a global dataset of 619 observations of four categories of organismal performance, spanning 14 phyla and 403 species. In agreement with both hypotheses, we show a positive relationship between the temperature of maximal performance rate (Topt) and environmental temperature (Tenv) for developmental rate and locomotion speed, but not growth or photosynthesis rate. Next, we demonstrate that relationships between Tenv and the maximal performance rate (Umax) are rarely significant and positive, as expected if a thermodynamic effect predominates. By contrast, a positive relationship between Topt and Umax is always present, but markedly weaker than theoretically predicted. These outcomes demonstrate that while some form of thermodynamic effect exists, ample scope is present for biochemical and physiological adaptation to thermal environments in the form of temperature compensation.

Original languageEnglish
Article number20181775
Number of pages10
JournalProceedings of the Royal Society B: Biological Sciences
Volume285
Issue number1890
DOIs
Publication statusPublished - 31 Oct 2018

Keywords

  • ectotherm
  • metabolic compensation
  • optimal temperature
  • physiological adaptation
  • thermodynamic effect

Cite this

@article{9d2b8c0330f847c2bf9ae63459d963b9,
title = "A widespread thermodynamic effect, but maintenance of biological rates through space across life's major domains",
abstract = "For over a century, the hypothesis of temperature compensation, the maintenance of similar biological rates in species from different thermal environments, has remained controversial. An alternative idea, that fitness is greater at higher temperatures (the thermodynamic effect), has gained increasing traction. This alternative hypothesis is also being used to understand large-scale biodiversity responses to environmental change. Yet evidence in favour of each of these contrasting hypotheses continues to emerge. In consequence, the fundamental nature of organismal thermal responses and its implications remain unresolved. Here, we investigate these ideas explicitly using a global dataset of 619 observations of four categories of organismal performance, spanning 14 phyla and 403 species. In agreement with both hypotheses, we show a positive relationship between the temperature of maximal performance rate (Topt) and environmental temperature (Tenv) for developmental rate and locomotion speed, but not growth or photosynthesis rate. Next, we demonstrate that relationships between Tenv and the maximal performance rate (Umax) are rarely significant and positive, as expected if a thermodynamic effect predominates. By contrast, a positive relationship between Topt and Umax is always present, but markedly weaker than theoretically predicted. These outcomes demonstrate that while some form of thermodynamic effect exists, ample scope is present for biochemical and physiological adaptation to thermal environments in the form of temperature compensation.",
keywords = "ectotherm, metabolic compensation, optimal temperature, physiological adaptation, thermodynamic effect",
author = "S{\o}rensen, {Jesper G.} and White, {Craig R.} and Duffy, {Grant A.} and Chown, {Steven L.}",
year = "2018",
month = "10",
day = "31",
doi = "10.1098/rspb.2018.1775",
language = "English",
volume = "285",
journal = "Proceedings of the Royal Society B: Biological Sciences",
issn = "0962-8452",
publisher = "The Royal Society Publishing",
number = "1890",

}

A widespread thermodynamic effect, but maintenance of biological rates through space across life's major domains. / Sørensen, Jesper G.; White, Craig R.; Duffy, Grant A.; Chown, Steven L.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 285, No. 1890, 20181775, 31.10.2018.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - A widespread thermodynamic effect, but maintenance of biological rates through space across life's major domains

AU - Sørensen, Jesper G.

AU - White, Craig R.

AU - Duffy, Grant A.

AU - Chown, Steven L.

PY - 2018/10/31

Y1 - 2018/10/31

N2 - For over a century, the hypothesis of temperature compensation, the maintenance of similar biological rates in species from different thermal environments, has remained controversial. An alternative idea, that fitness is greater at higher temperatures (the thermodynamic effect), has gained increasing traction. This alternative hypothesis is also being used to understand large-scale biodiversity responses to environmental change. Yet evidence in favour of each of these contrasting hypotheses continues to emerge. In consequence, the fundamental nature of organismal thermal responses and its implications remain unresolved. Here, we investigate these ideas explicitly using a global dataset of 619 observations of four categories of organismal performance, spanning 14 phyla and 403 species. In agreement with both hypotheses, we show a positive relationship between the temperature of maximal performance rate (Topt) and environmental temperature (Tenv) for developmental rate and locomotion speed, but not growth or photosynthesis rate. Next, we demonstrate that relationships between Tenv and the maximal performance rate (Umax) are rarely significant and positive, as expected if a thermodynamic effect predominates. By contrast, a positive relationship between Topt and Umax is always present, but markedly weaker than theoretically predicted. These outcomes demonstrate that while some form of thermodynamic effect exists, ample scope is present for biochemical and physiological adaptation to thermal environments in the form of temperature compensation.

AB - For over a century, the hypothesis of temperature compensation, the maintenance of similar biological rates in species from different thermal environments, has remained controversial. An alternative idea, that fitness is greater at higher temperatures (the thermodynamic effect), has gained increasing traction. This alternative hypothesis is also being used to understand large-scale biodiversity responses to environmental change. Yet evidence in favour of each of these contrasting hypotheses continues to emerge. In consequence, the fundamental nature of organismal thermal responses and its implications remain unresolved. Here, we investigate these ideas explicitly using a global dataset of 619 observations of four categories of organismal performance, spanning 14 phyla and 403 species. In agreement with both hypotheses, we show a positive relationship between the temperature of maximal performance rate (Topt) and environmental temperature (Tenv) for developmental rate and locomotion speed, but not growth or photosynthesis rate. Next, we demonstrate that relationships between Tenv and the maximal performance rate (Umax) are rarely significant and positive, as expected if a thermodynamic effect predominates. By contrast, a positive relationship between Topt and Umax is always present, but markedly weaker than theoretically predicted. These outcomes demonstrate that while some form of thermodynamic effect exists, ample scope is present for biochemical and physiological adaptation to thermal environments in the form of temperature compensation.

KW - ectotherm

KW - metabolic compensation

KW - optimal temperature

KW - physiological adaptation

KW - thermodynamic effect

UR - http://www.scopus.com/inward/record.url?scp=85055834619&partnerID=8YFLogxK

U2 - 10.1098/rspb.2018.1775

DO - 10.1098/rspb.2018.1775

M3 - Article

VL - 285

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1890

M1 - 20181775

ER -