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Comparative Study
. 2016 May 19;533(7603):390-2.
doi: 10.1038/nature17654. Epub 2016 May 4.

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

Herman Pontzer  1   2 , Mary H Brown  3 , David A Raichlen  4 , Holly Dunsworth  5 , Brian Hare  6 , Kara Walker  6 , Amy Luke  7 , Lara R Dugas  7 , Ramon Durazo-Arvizu  7 , Dale Schoeller  8 , Jacob Plange-Rhule  9 , Pascal Bovet  10   11 , Terrence E Forrester  12 , Estelle V Lambert  13 , Melissa Emery Thompson  14 , Robert W Shumaker  15   16   17 , Stephen R Ross  3
Affiliations
Comparative Study

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

Herman Pontzer et al. Nature. .

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 longevity. 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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Figures

Extended Data Figure 1
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 wild (see Supplementary Table 2).
Extended Data Figure 2
Extended Data Figure 2. BMRs for humans, chimpanzees and orangutans
Available BMR data for chimpanzees, are primarily from juveniles (age: 2 months to 15 years), and are shown here against comparably aged humans (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 individual (no age reported, mass 16.2 kg). Resting metabolic rates (RMRs; kcal day−1), measured in alert orangutans while sitting, are also shown. The top of the bar indicates the measured RMR for those individuals, and the bottom square indicates estimated BMR bas ed on those measurements, 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 adults.
Figure 1
Figure 1. TTE and FFM for hominoids
Humans (Homo, grey, n = 141), chimpanzees and bonobos (Pan, blue, n = 35), gorillas (Gorilla, green, n = 10), and orangutans (Pongo, orange, n = 11). Lines and shaded regions indicate least squares regressions and 95% confidence intervals for each genus. TEE for Homo exceeds other genera in a general linear model accounting for FFM, fat mass and other variables (P 0.001; Table 1 and Supplementary Table 3).
Figure 2
Figure 2. Predicted TEE, BMR and fat mass for adult hominoids
Values are estimated for males (55 kg FFM) and females (45 kg FFM), using the same FFM across genera. TEE (red bars) is estimated from FFM, fat mass and genus using model C in Supplementary Table 3; error bars represent model standard error. BMR (darker red regions) is estimated from body mass (Methods and Extended Data Fig. 2); no BMR data are available for Gorilla. Fat mass (yellow bars) is calculated from FFM using body fat percentages in Table 1.
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