Skip to main content
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian
  • Log in
  • My Cart

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses

New Research In

Physical Sciences

Featured Portals

  • Physics
  • Chemistry
  • Sustainability Science

Articles by Topic

  • Applied Mathematics
  • Applied Physical Sciences
  • Astronomy
  • Computer Sciences
  • Earth, Atmospheric, and Planetary Sciences
  • Engineering
  • Environmental Sciences
  • Mathematics
  • Statistics

Social Sciences

Featured Portals

  • Anthropology
  • Sustainability Science

Articles by Topic

  • Economic Sciences
  • Environmental Sciences
  • Political Sciences
  • Psychological and Cognitive Sciences
  • Social Sciences

Biological Sciences

Featured Portals

  • Sustainability Science

Articles by Topic

  • Agricultural Sciences
  • Anthropology
  • Applied Biological Sciences
  • Biochemistry
  • Biophysics and Computational Biology
  • Cell Biology
  • Developmental Biology
  • Ecology
  • Environmental Sciences
  • Evolution
  • Genetics
  • Immunology and Inflammation
  • Medical Sciences
  • Microbiology
  • Neuroscience
  • Pharmacology
  • Physiology
  • Plant Biology
  • Population Biology
  • Psychological and Cognitive Sciences
  • Sustainability Science
  • Systems Biology
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;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • 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;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • 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;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Marcel G. Brown
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Alan M. Batterham
eSchool of Health and Social Care, Teeside University, TS1 3BX Middlesbrough, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Steven Worthington
fInstitute for Quantitative Social Science, Harvard University, Cambridge, MA 02138;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • 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
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yedra Feltrer
cInternational Primate Heart Project, Cardiff Metropolitan University, CF23 6XD Cardiff, United Kingdom;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jennifer Neary
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rory B. Weiner
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Meagan M. Wasfy
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Aaron L. Baggish
dCardiovascular Performance Program, Division of Cardiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • 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

See related content:

  • Reply to Jensen and Wang: Chimpanzees under pressure—Selection of a left ventricular structural and functional phenotype
    - Feb 20, 2020
  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Article Figures & SI

Figures

  • Tables
  • Fig. 1.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 1.

    Comparison of the LV structure and the function in chimpanzees and 2 representative human groups: sedentary Americans and Tarahumara subsistence farmers. (A–C) Scaled outlines of LVs among the 3 groups highlighting differences in trabeculation, WT, chamber size, and shape. (D) Basal and apical systolic (shaded) and diastole (unshaded) rotation. (E) Magnitude of LV twisting, untwisting, and the respective velocities during systole (shaded) and diastole (unshaded). While chimpanzees lack apical rotation and, thus, overall systolic twist, sedentary humans and subsistence farmers have similar levels of systolic twisting and early diastolic UTVs.

  • Fig. 2.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 2.

    Comparison of the LV structure and the function among chimpanzees and 4 human groups with diverse physical activity histories. (A and B) Principal component analysis of LV variables determined a priori to be associated with either pressure (A) or volume (B) exposure. Principal component scores are expressed as standardized Z scores. (C and D) General linear model of first principal component scores for pressure (C) and volume (D) regressed on group identity with means and 95% confidence intervals. Groups analyzed: chimpanzees (CHI); sedentary Americans (SAM); American-style football linemen (AFL); long-distance runners (LDR); and Tarahumara subsistence farmers (TAR). Pressure variables are as follows: peak systolic LV tissue velocity (S′), Mid-LV Mid RWT, basal-LV RWT, Mid-LV Mid WT, SBP, DBP; volume variables are early diastolic transmitral valve blood flow velocity (MVE), peak early diastolic tissue velocity (E′), SI, CO, SV, LVL, LV EDV, LV ESV, LV OT diameter. All ventricular structural data entered into the analyses were scaled as per SI Appendix.

  • Fig. 3.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 3.

    Trade-off between EPA and RPA training on the LV structure and function. (A) After 90 d of intensive training, the EPA athletes demonstrated eccentric LV remodeling characterized by increases in LV chamber volume (∆ EDV = 7%, ∆ RWT = −3%) and improved diastolic function (∆ E′ = 12%) while the RPA athletes demonstrated concentric remodeling characterized by (∆ WT = 13%, ∆ RWT = 8%) and reduced diastolic function (∆ E′ = −7%). (B) Relationship between RWT and LV SV in response to volume challenge (Top) and pressure challenge (Bottom) among these athletes after training. RPA-trained athletes with relatively thicker LV walls were less able than EPA-trained athletes to increase SV (∆SV = 6% vs. ∆SV = 16%) when challenged with rapid intravascular infusion of normal saline. In contrast, RPA-trained athletes were better able to preserve SV (∆SV = −4%) when pressure challenged with an isometric grip test than EPA-trained athletes (∆SV = −21%).

  • Fig. 4.
    • Download figure
    • Open in new tab
    • Download powerpoint
    Fig. 4.

    Difference in SBP (solid line) and DBP (dashed line) in male chimpanzees, Tarahumara subsistence farmers, and sedentary Americans (NHANES data). Tarahumara subsistence farmers (blue) and sedentary Americans (green) are presented relative to age (shaded areas indicate 95% confidence interval of the mean), whereas a point estimate of mean BP relative to mean age is provided for the smaller chimpanzee cohort (red). Although BP increases with age in the NHANES sample, this is not apparent in the Tarahumara.

Tables

  • Figures
    • View popup
    Table 1.

    Demographic, hemodynamic, and LV structure and function (scaled where appropriate) in semiwild sanctuary chimpanzees, Tarahumara, sedentary humans, LDRs, and American football linemen (AFL)

    Parameter assessedChimpanzeees (n = 43)All humans (n = 164)Tarahumara (n = 42)Sedentary humans (n = 40)LDRs (n = 42)AFL (n = 40)P value*
    Demographics
     Age (years)21 ± 525 ± 833 ± 8†27 ± 4†20 ± 219 ± 10.015
     Body Mass (kg)55 ± 876 ± 1862 ± 8†75 ± 9†67 ± 5†102 ± 14†<0.001
     Height (cm)‡127 ± 9176 ± 10164 ± 5†176 ± 7†179 ± 6†185 ± 9†<0.001
    Hemodynamics
     SBP (mmHg)138 ± 21116 ± 11113 ± 11†115 ± 8†110 ± 8†127 ± 9<0.001
     DBP (mmHg)92 ± 1767 ± 1169 ± 10†67 ± 8†60 ± 8†74 ± 13†<0.001
     Heart rate/mass−0.25158 ± 28178 ± 31165 ± 26179 ± 24†159 ± 24209 ± 24†0.002
     CO (L/min)/mass0.750.147 ± 0.0470.208 ± 0.0490.181 ± 0.036†0.188 ± 0.035†0.250 ± 0.047†0.210 ± 0.045†<0.001
    LV structure
     Mid-LV WT (cm)/mass0.250.376 ± 0.0890.307 ± 0.0530.264 ± 0.033†0.323 ± 0.039†0.274 ± 0.026†0.372 ± 0.024<0.001
     Mid-LV RWT0.427 ± 0.1130.366 ± 0.0740.317 ± 0.058†0.378 ± 0.0500.322 ± 0.035†0.452 ± 0.0580.02
     EDV (ml)/mass1.01.8 ± 0.32.0 ± 0.51.7 ± 0.31.7 ± 0.32.8 ± 0.3†1.7 ± 0.20.201
     ESV (ml)/mass1.00.91 ± 0.240.79 ± 0.290.63 ± 0.14†0.63 ± 0.15†1.20 ± 0.18†0.68 ± 0.12†0.095
     LVL (cm)/mass0.252.80 ± 0.203.00 ± 0.293.11 ± 015†2.79 ± 0.203.31 ± 0.20†2.78 ± 0.16<0.001
     LV OT (cm)/mass0.250.720 ± 0.0630.728 ± 0.0550.755 ± 0.0430.698 ± 0.0460.768 ± 0.039†0.688 ± 0.0431
     SI1.68 ± 0.151.85 ± 0.171.90 ± 0.16†1.84 ± 0.11†1.93 ± 0.15†1.72 ± 0.17<0.001
    LV Systolic function
     SV (ml)/mass1.00.926 ± 0.2191.192 ± 0.3041.109 ± 0.194†1.057 ± 0.1941.578 ± 0.205†1.006 ± 0.197<0.001
     S′ (cm/s)0.0624 ± 0.01340.1114 ± 0.01570.1015 ± 0.0157†0.1143 ± 0.0093†0.1067 ± 0.0146†0.1235 ± 0.0133†<0.001
     Peak LV twist (°)§6.4 ± 3.317.4 ± 6.218.0 ± 6.3†18.4 ± 5.7†14.4 ± 5.2†16.5 ± 7.4†<0.001
    LV diastolic function
     E (cm/s)0.77 ± 0.170.83 ± 0.140.85 ± 0.200.84 ± 0.110.88 ± 0.130.77 ± 0.090.241
     A (cm/s)0.39 ± 0.150.51 ± 0.150.51 ± 0.15†0.48 ± 0 0.11†0.39 ± 0.090.65 ± 0.14†<0.001
     E/A2.21 ± 0.731.82 ± 0.691.79 ± 0.651.82 ± 0.442.38 ± 0.731.26 ± 0.38†0.029
     E′ (cm/s)0.101 ± 0.0240.136 ± 0.0320.152 ± 0.030†0.115 ± 0.0140.168 ± 0.013†0.107 ± 0.018<0.001
     A′ (cm/s)0.062 ± 0.0180.073 ± 0.0250.102 ± 0.020†0.051 ± 0.0120.065 ± 0.0110.074 ± 0.0200.017
     LV UTV (°/s)§−53 ± 23−109 ± 38−109 ± 39†−121 ± 44†−109 ± 27†−96 ± 36†<0.001
    • SBP, systolic blood pressure; DBP, diastolic blood pressure; CO, cardiac output; LV, left ventricular; WT, wall thickness; RWT, relative WT; EDV, end diastolic volume; ESV, end systolic volume; OT, outflow tract; SV, stroke volume; S′, systolic ventricular wall velocity; LVL, LV length; E, early diastolic transmitral filling velocity; A, late diastolic transmitral filling velocity; E:A, the ratio of early to late diastolic transmitral filling velocities; E′, early diastolic ventricular wall velocity; A′, late diastolic ventricular wall velocity; UTV, untwisting velocity.

    • ↵* Comparison of chimpanzees to all humans using 2-tailed unpaired Welch’s t tests for unequal variances. P values are adjusted for familywise error (37 tests) using the sequential Bonferroni method.

    • ↵† P < 0.05 for comparison of chimpanzees to individual human groups using 2-tailed unpaired Welch’s t tests for unequal variances. P values are adjusted for familywise error (148 tests) using the sequential Bonferroni method.

    • ↵‡ Calculated via the summation of lower limb and crown to rump measurements. n = 207 for all analyses except: EDV/mass1.0 (198); ESV/mass1.0 (198); SV/mass1.0 (198); CO/mass0.75 (198); sphericity index (SI) (204); MVE (206); MVA (206); MV E/A (206); mean E′ (206); mean A′ (206); mean S′ (205); twist peak (97); UTV (97). See SI Appendix for full table including all nonscaled variables.

    • ↵§ For 2 angular variables (peak LV twist and LV UTV) a circular-linear model with a von Mises distribution for the response was used to compare means across groups.

Data supplements

  • Supporting Information

    • Download Appendix (PDF)
PreviousNext
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Selection of endurance capabilities and the trade-off between pressure and volume in the evolution of the human heart
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
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

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
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
Digg logo Reddit logo Twitter logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 116 (40)
Table of Contents

Submit

Sign up for Article Alerts

Article Classifications

  • Biological Sciences
  • Anthropology

Jump to section

  • Article
    • Abstract
    • Results
    • Discussion
    • Materials and Methods
    • Acknowledgments
    • Footnotes
    • References
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Surgeons hands during surgery
Inner Workings: Advances in infectious disease treatment promise to expand the pool of donor organs
Despite myriad challenges, clinicians see room for progress.
Image credit: Shutterstock/David Tadevosian.
Setting sun over a sun-baked dirt landscape
Core Concept: Popular integrated assessment climate policy models have key caveats
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Double helix
Journal Club: Noncoding DNA shown to underlie function, cause limb malformations
Using CRISPR, researchers showed that a region some used to label “junk DNA” has a major role in a rare genetic disorder.
Image credit: Nathan Devery.
Steamboat Geyser eruption.
Eruption of Steamboat Geyser
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Listen
Past PodcastsSubscribe
Multi-color molecular model
Enzymatic breakdown of PET plastic
A study demonstrates how two enzymes—MHETase and PETase—work synergistically to depolymerize the plastic pollutant PET.
Image credit: Aaron McGeehan (artist).

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490