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Research Article

Selection of endurance capabilities and the trade-off between pressure and volume in the evolution of the human heart

Robert E. Shave, Daniel E. Lieberman, Aimee L. Drane, Marcel G. Brown, Alan M. Batterham, View ORCID ProfileSteven Worthington, Rebeca Atencia, Yedra Feltrer, Jennifer Neary, Rory B. Weiner, Meagan M. Wasfy, and Aaron L. Baggish
PNAS October 1, 2019 116 (40) 19905-19910; first published September 16, 2019; https://doi.org/10.1073/pnas.1906902116
Robert E. Shave
aCentre for Heart, Lung and Vascular Health, School of Health and Exercise Sciences, University of British Columbia, Kelowna, BC V1V 1V7, Canada;
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  • For correspondence: rob.shave@ubc.ca danlieb@fas.harvard.edu ABAGGISH@mgh.harvard.edu
Daniel E. Lieberman
bDepartment of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138;
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  • For correspondence: rob.shave@ubc.ca danlieb@fas.harvard.edu ABAGGISH@mgh.harvard.edu
Aimee L. Drane
cInternational Primate Heart Project, Cardiff Metropolitan University, CF23 6XD Cardiff, United Kingdom;
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Marcel G. Brown
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
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Alan M. Batterham
eSchool of Health and Social Care, Teeside University, TS1 3BX Middlesbrough, United Kingdom;
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Steven Worthington
fInstitute for Quantitative Social Science, Harvard University, Cambridge, MA 02138;
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  • ORCID record for Steven Worthington
Rebeca Atencia
cInternational Primate Heart Project, Cardiff Metropolitan University, CF23 6XD Cardiff, United Kingdom;
gJane Goodall Institute, Tchimpounga Chimpanzee Rehabilitation Centre, Republic of Congo
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Yedra Feltrer
cInternational Primate Heart Project, Cardiff Metropolitan University, CF23 6XD Cardiff, United Kingdom;
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Jennifer Neary
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
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Rory B. Weiner
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
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Meagan M. Wasfy
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
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Aaron L. Baggish
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
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  • For correspondence: rob.shave@ubc.ca danlieb@fas.harvard.edu ABAGGISH@mgh.harvard.edu
  1. Edited by Christopher W. Kuzawa, Northwestern University, Evanston, IL, and approved August 8, 2019 (received for review April 23, 2019)

This article has a Letter. Please see:

  • Apes, adaptations, and artifacts of anesthetics - February 20, 2020

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  • Reply to Jensen and Wang: Chimpanzees under pressure—Selection of a left ventricular structural and functional phenotype
    - Feb 20, 2020
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Significance

Unlike other great apes, humans evolved multisystem capabilities for moderate-intensity EPA, but it is unknown if selection acted similarly on the heart. We present data from a sample of humans, chimpanzees, and gorillas showing that the human (LV) evolved numerous features that help to augment stroke volume (SV), enabling moderate-intensity EPA. We also show that phenotypic plasticity of the human LV trades off pressure adaptations for volume capabilities, becoming more similar to a chimpanzee-like heart in response to physical inactivity or chronic pressure loading. Consequently, the derived human heart appears partly dependent upon moderate EPA and its absence, in combination with a highly processed diet, likely contributes to the modern epidemic of hypertensive heart disease.

Abstract

Chimpanzees and gorillas, when not inactive, engage primarily in short bursts of resistance physical activity (RPA), such as climbing and fighting, that creates pressure stress on the cardiovascular system. In contrast, to initially hunt and gather and later to farm, it is thought that preindustrial human survival was dependent on lifelong moderate-intensity endurance physical activity (EPA), which creates a cardiovascular volume stress. Although derived musculoskeletal and thermoregulatory adaptations for EPA in humans have been documented, it is unknown if selection acted similarly on the heart. To test this hypothesis, we compared left ventricular (LV) structure and function across semiwild sanctuary chimpanzees, gorillas, and a sample of humans exposed to markedly different physical activity patterns. We show the human LV possesses derived features that help augment cardiac output (CO) thereby enabling EPA. However, the human LV also demonstrates phenotypic plasticity and, hence, variability, across a wide range of habitual physical activity. We show that the human LV’s propensity to remodel differentially in response to chronic pressure or volume stimuli associated with intense RPA and EPA as well as physical inactivity represents an evolutionary trade-off with potential implications for contemporary cardiovascular health. Specifically, the human LV trades off pressure adaptations for volume capabilities and converges on a chimpanzee-like phenotype in response to physical inactivity or sustained pressure loading. Consequently, the derived LV and lifelong low blood pressure (BP) appear to be partly sustained by regular moderate-intensity EPA whose decline in postindustrial societies likely contributes to the modern epidemic of hypertensive heart disease.

  • blood pressure
  • physical activity
  • left ventricle
  • trade-off
  • human evolution

Footnotes

  • ↵1To whom correspondence may be addressed. Email: rob.shave{at}ubc.ca, danlieb{at}fas.harvard.edu, or ABAGGISH{at}mgh.harvard.edu.
  • Author contributions: R.E.S., D.E.L., and A.L.B. designed research; R.E.S., D.E.L., A.L.D., M.G.B., R.A., Y.F., J.N., R.B.W., M.M.W., and A.L.B. performed research; R.E.S., D.E.L., A.L.D., A.M.B., S.W., R.B.W., and A.L.B. analyzed data; and R.E.S., D.E.L., and A.L.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1906902116/-/DCSupplemental.

  • Copyright © 2019 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Selection of endurance capabilities and the trade-off between pressure and volume in the evolution of the human heart
Robert E. Shave, Daniel E. Lieberman, Aimee L. Drane, Marcel G. Brown, Alan M. Batterham, Steven Worthington, Rebeca Atencia, Yedra Feltrer, Jennifer Neary, Rory B. Weiner, Meagan M. Wasfy, Aaron L. Baggish
Proceedings of the National Academy of Sciences Oct 2019, 116 (40) 19905-19910; DOI: 10.1073/pnas.1906902116

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Selection of endurance capabilities and the trade-off between pressure and volume in the evolution of the human heart
Robert E. Shave, Daniel E. Lieberman, Aimee L. Drane, Marcel G. Brown, Alan M. Batterham, Steven Worthington, Rebeca Atencia, Yedra Feltrer, Jennifer Neary, Rory B. Weiner, Meagan M. Wasfy, Aaron L. Baggish
Proceedings of the National Academy of Sciences Oct 2019, 116 (40) 19905-19910; DOI: 10.1073/pnas.1906902116
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