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Metabolic acceleration and the evolution of human brain size and life history

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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Figure 1: TTE and FFM for hominoids.
Figure 2: Predicted TEE, BMR and fat mass for adult hominoids.

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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.

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Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Herman Pontzer.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 The human energetic paradox.

Humans achieve greater reproductive output (g year−1; black bar) and have larger brains (g; blue bar) relative to female metabolic mass (kg0.75) than any of the great apes, yet also achieve longer lifespans (grey bar). Human data are from traditional hunter–gatherer and subsistence farming populations; ape data are from populations in the wild1 (see Supplementary Table 2).

Extended Data Figure 2 BMRs for humans, chimpanzees and orangutans.

Available BMR data for chimpanzees15,16 are primarily from juveniles (age: 2 months to 15 years), and are shown here against comparably aged humans14 (3–18 years). Humans have greater BMRs than chimpanzees in a general linear model of ln-transformed BMR and mass controlling for age and sex (P < 0.001; Supplementary Table 3). Note that in humans (but not chimpanzees), males have greater BMRs for a given body mass, reflecting their greater proportion of FFM (that is, lower body fat percentage). The available data for orangutan BMR consists of one juvenile individual16 (no age reported, mass 16.2 kg). Resting metabolic rates (RMRs; kcal day−1), measured in alert orangutans while sitting17, are also shown. The top of the bar indicates the measured RMR for those individuals, and the bottom square indicates estimated BMR based on those measurements17, assuming BMR = 0.8RMR. No BMR data are available for gorillas. Symbols marked with black circles are males. Allometric regressions shown for Pan (y = 100.17x0.65) and Pongo (y = 218.61x0.37) and were used to estimate BMR for the adult cohorts in Table 1. Human BMR in Table 1 was estimated from published, sex-specific predictive equations for adults27.

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Pontzer, H., Brown, M., Raichlen, D. et al. Metabolic acceleration and the evolution of human brain size and life history. Nature 533, 390–392 (2016). https://doi.org/10.1038/nature17654

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