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.

Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates' slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates' slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates' slow metabolic rates contribute to their characteristically slow life histories.metabolism | evolution | ecology T he pace at which organisms grow, reproduce, and age must ultimately reflect their physiological energy expenditure; growth of new tissue (self or offspring) and the maintenance and repair of the body all require metabolic investment. In principle, either the total energy budget, also called "total energy expenditure" (TEE) (kilocalories per day), or allocation within the energy budget could change over evolutionary time to fuel changes in life history schedules. Studies of mammalian life history have generally focused on variation in allocation (1-6), in part because of the lack of evidence correlating gross measures of energy expenditure with life history. The basal metabolic rate (BMR) (kilocalories per day), often used as an index of the total energy budget, is unrelated to rates of growth, reproduction, or aging among placental mammals when accounting for the effects of body mass and phylogenetic relatedness (7-9). The focus on allocation is also consistent with evidence, albeit mixed, for evolved tradeoffs among metabolically expensive organs (10,11) and between metabolically expensive organs and reproductive output (12).Variation in allocation undoubtedly affects life history schedules, but the use of BMR as a measure of the energy budget may obscure the complementary role of variation in energy throughput. For example, senescence due to the production of free radicals and other metabolic damage is a consequence of TEE, not only the portion expended on BMR (7). Further, because BMR accounts for less than half of TEE for most mammals (13), analyses of BMR do not reflect the full amount of energy potentially available for growth and reproduction. Indeed, the relationship bet...