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A century of exercise physiology: concepts that ignited the study of human thermoregulation. Part 4: evolution, thermal adaptation and unsupported theories of thermoregulation

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Abstract

This review is the final contribution to a four-part, historical series on human exercise physiology in thermally stressful conditions. The series opened with reminders of the principles governing heat exchange and an overview of our contemporary understanding of thermoregulation (Part 1). We then reviewed the development of physiological measurements (Part 2) used to reveal the autonomic processes at work during heat and cold stresses. Next, we re-examined thermal-stress tolerance and intolerance, and critiqued the indices of thermal stress and strain (Part 3). Herein, we describe the evolutionary steps that endowed humans with a unique potential to tolerate endurance activity in the heat, and we examine how those attributes can be enhanced during thermal adaptation. The first of our ancestors to qualify as an athlete was Homo erectus, who were hairless, sweating specialists with eccrine sweat glands covering almost their entire body surface. Homo sapiens were skilful behavioural thermoregulators, which preserved their resource-wasteful, autonomic thermoeffectors (shivering and sweating) for more stressful encounters. Following emigration, they regularly experienced heat and cold stress, to which they acclimatised and developed less powerful (habituated) effector responses when those stresses were re-encountered. We critique hypotheses that linked thermoregulatory differences to ancestry. By exploring short-term heat and cold acclimation, we reveal sweat hypersecretion and powerful shivering to be protective, transitional stages en route to more complete thermal adaptation (habituation). To conclude this historical series, we examine some of the concepts and hypotheses of thermoregulation during exercise that did not withstand the tests of time.

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Fig. 1

Source: Used with permission of The Comrades Marathon Association, which retains copyright. B Zasson (Jason) Zirganos (Greece) at the completion if his English Channel swim from Dungeness Point (France) to Folkestone (England; 1951 [14 h 10 min]). Source: https://www.channelswimmingdover.org.uk/content/photo/major-jason-zirganos-of-greece-with-sam-rockett Accessed: July 11th, 2022. This photograph is in the Public Domain

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Source: Royalty-free image from Pixabay. B Chimpanzee offspring also cling, but mothers assist very young offspring with an arm; locomotion is then more difficult. Source: Royalty-free image from Pixabay. C: Human infants cannot cling, but our upright posture, which freed the arms, made offspring carriage possible. Source: Netpix.com (https://www.needpix.com/photo/1345586/), used under Creative Commons Zero License for Public Domain

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Source: Singapore Medical Journal (Merritt and Tan 2011). Accessed: March 17th, 2022

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Source: https://www.loc.gov/item/2001705606/ Accessed: March 17th, 2022. B Two Inuit women from Greenland, after spending four days in a portable, open-circuit respirometer. Photograph taken in 1908 during the Danish expedition to the northeast coast, and extracted from the report of Krogh and Krogh (1913). Source: https://archive.org/details/studyofdietmetab51krog/page/n9/mode/2up?ref=ol&view=theater&pg=PA18 Accessed: March 17th, 2022. C Variations in ethnic differences in mass-specific surface area associated with climatic differences. Data were extracted from Forster and Collard (2013), redrawn and re-analysed to show a linear function with 95% confidence intervals

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Source: University of Adelaide (2013: http://www.adelaide.edu.au/library/special/mss/hicks/). Both photographs are in the Public Domain

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Modified from Patterson et al. (2004a)

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Abbreviations

T b-i :

Body temperature at time i

T b-0 :

Basal body temperature

dt :

The duration of the thermal stimulus

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Acknowledgements

SRN was supported by a Postdoctoral Fellowship from the Human and Environmental Physiology Research Unit, University of Ottawa (Canada), during the developmental stages of this work. The authors acknowledge contributions from Shane K. Maloney, Edward Snelling, Michael Kearney and Andrea Fuller, and the libraries of the University of Western Australia and the University of the Witwatersrand during the writing of this manuscript. We again acknowledge the many and varied, but always significant, contributions of our friends in science (also known as students and colleagues). Finally, and by no means least, we thank our long-suffering families and unscientific friends for their patience during this marathon (or was it four marathons?).

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Authors and Affiliations

  1. Defence Science and Technology Group, Department of Defence, Melbourne, Australia

    Sean R. Notley

  2. Brain Function Research Group, School of Physiology, University of the Witwatersrand, Johannesburg, South Africa

    Duncan Mitchell

  3. School of Human Sciences, University of Western Australia, Crawley, Australia

    Duncan Mitchell

  4. Research Institute of Human Ecology, College of Human Ecology, Seoul National University, Seoul, Republic of Korea

    Nigel A. S. Taylor

  5. School of Human Kinetics, University of Ottawa, Ottawa, Canada

    Sean R. Notley

Authors
  1. Sean R. Notley
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  2. Duncan Mitchell
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  3. Nigel A. S. Taylor
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Contributions

SRN, DM and NAST: developed and planned this review, and took part in all phases of manuscript preparation. Each author was responsible for writing specific sub-sections, and for editing all parts of this work. All authors approved the final submission of this manuscript.

Corresponding author

Correspondence to Nigel A. S. Taylor.

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Communicated by Michael I Lindinger.

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Notley, S.R., Mitchell, D. & Taylor, N.A.S. A century of exercise physiology: concepts that ignited the study of human thermoregulation. Part 4: evolution, thermal adaptation and unsupported theories of thermoregulation. Eur J Appl Physiol 124, 147–218 (2024). https://doi.org/10.1007/s00421-023-05262-9

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  • DOI: https://doi.org/10.1007/s00421-023-05262-9

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