Abstract

Humans are distinguished from the other living apes in having larger brains and an unusual life history that combines high reproductive output with slow childhood growth and exceptional longevity1. This suite of derived traits suggests major changes in energy expenditure and allocation in the human lineage, but direct measures of human and ape metabolism are needed to compare evolved energy strategies among hominoids. Here we used doubly labelled water measurements of total energy expenditure (TEE; kcal day−1) in humans, chimpanzees, bonobos, gorillas and orangutans to test the hypothesis that the human lineage has experienced an acceleration in metabolic rate, providing energy for larger brains and faster reproduction without sacrificing maintenance and longevity. In multivariate regressions including body size and physical activity, human TEE exceeded that of chimpanzees and bonobos, gorillas and orangutans by approximately 400, 635 and 820 kcal day−1, respectively, readily accommodating the cost of humans’ greater brain size and reproductive output. Much of the increase in TEE is attributable to humans’ greater basal metabolic rate (kcal day−1), indicating increased organ metabolic activity. Humans also had the greatest body fat percentage. An increased metabolic rate, along with changes in energy allocation, was crucial in the evolution of human brain size and life history.

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Acknowledgements

We thank participating zoos and staff for their efforts: Houston Zoo, Indianapolis Zoo, Jacksonville Zoo, Lincoln Park Zoo, Milwaukee County Zoo, North Carolina Zoo, Oklahoma City Zoo, Oregon Zoo, Zoo Atlanta, Woodland Park Zoo, Dallas Zoo, Brookfield Zoo and Columbus Zoo. We thank B. Moumbaka for assistance administering doses and collecting samples for analysis. We thank R. Atencia and C. Andre for supporting this project. Work at Tchimpounga and Lola Ya Bonobo was performed under the authority of the Ministry of Research and the Ministry of Environment in the Democratic Republic of Congo (research permit #MIN.RS/SG/004/ 2009) and the Ministry of Scientific Research and Technical Innovation in the Congo Republic (research permit 09/MRS/DGRST/ DMAST), with samples imported under CITES permits 09US223466/9 and 9US207589/9. L. Christopher, K. Stafford and J. Paltan assisted with sample analyses. Funding was provided by the US National Science Foundation (BCS-1317170), National Institutes of Health (R01DK080763), L.S.B. Leakey Foundation, Wenner-Gren Foundation (Gr. 8670), University of Arizona and Hunter College.

Author information

Affiliations

  1. Department of Anthropology, Hunter College. 695 Park Avenue, New York, New York 10065, USA

    • Herman Pontzer
  2. New York Consortium for Evolutionary Primatology, New York, New York 10065, USA

    • Herman Pontzer
  3. Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo. Chicago, Illinois 60614, USA

    • Mary H. Brown
    •  & Stephen R. Ross
  4. School of Anthropology, University of Arizona, 1099 E South Campus Drive, Tucson, Arizona 85716, USA

    • David A. Raichlen
  5. Department of Sociology & Anthropology, University of Rhode Island, 45 Upper College Rd, Kingston, Rhode Island 02881, USA

    • Holly Dunsworth
  6. Department of Evolutionary Anthropology, Duke University, Durham, North Carolina 27708, USA

    • Brian Hare
    •  & Kara Walker
  7. Public Health Sciences, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, Illinois 60153, USA

    • Amy Luke
    • , Lara R. Dugas
    •  & Ramon Durazo-Arvizu
  8. Nutritional Sciences, Biotechnology Center, University of Wisconsin–Madison, 425 Henry Mall, Madison, Wisconsin 53705, USA

    • Dale Schoeller
  9. Kwame Nkrumah University of Science and Technology, Kumasi, Ghana

    • Jacob Plange-Rhule
  10. Institute of Social & Preventive Medicine, Lausanne University Hospital, Rue de la Corniche 10, 1010 Lausanne, Switzerland

    • Pascal Bovet
  11. Ministry of Health, PO Box 52, Victoria, Mahé, Seychelles

    • Pascal Bovet
  12. UWI Solutions for Developing Countries, The University of the West Indies, 25 West Road, UWI Mona Campus, Kingston 7, Jamaica

    • Terrence E. Forrester
  13. Research Unit for Exercise Science and Sports Medicine, University of Cape Town, PO Box 115, Newlands 7725, Cape Town, South Africa

    • Estelle V. Lambert
  14. Department of Anthropology, University of New Mexico. Albuquerque, New Mexico 87131, USA

    • Melissa Emery Thompson
  15. Indianapolis Zoo, 1200 W Washington Street, Indianapolis, Indiana 46222, USA

    • Robert W. Shumaker
  16. Department of Anthropology and Center for Integrated Study of Animal Behavior, Indiana University, 701 E Kirkwood Avenue, Bloomington, Indiana 47405, USA

    • Robert W. Shumaker
  17. Krasnow Institute for Advanced Study, George Mason University, 4400 University Dr., Fairfax, Virginia 22030, USA

    • Robert W. Shumaker

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Contributions

H.P. and S.R.R. designed the study; H.P., M.H.B., D.A.R., H.D., B.H., K.W., A.L., L.R.D., J.P.-R., P.B., T.E.F., E.V.L., R.W.S. and S.R.R. collected data; H.P., R.D.-A., M.E.T. and D.S. analysed data. All authors contributed to writing the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Herman Pontzer.

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DOI

https://doi.org/10.1038/nature17654

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