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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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.
Extended data figures
This file contains Supplementary Text and Data, Supplementary Tables 1-3, Supplementary Figures 1-2 and additional references.