Primate energy expenditure and life history

Abstract

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.

Keywords: ecology; evolution; metabolism.

Fig. 1.

Primate TEE and BMR. (A) TEE vs. body mass for primates (red, n = 17 species, 19 populations) and nonprimate eutherian mammals (gray, n = 67); shaded areas indicate 95% confidence regions for the ordinary least squares (OLS) regressions. The dotted line represents primate OLS regression excluding mouse lemurs. Open primate symbols indicate captive primate populations. (B) Density plots of standardized residuals (Z scores) from the nonprimate regression. ANCOVA and residuals show a significant shift in TEE for primates (SI Text, section 2 and Fig. S1). (C) BMR vs. body mass; symbols as in A (n = 43 primates, 407 nonprimates). (D) Standardized residuals (Z scores) from the nonprimate BMR regression.

Fig. 2.

Primate life history and TEE. Life history traits (9) for primates (red) and other eutherian mammals (gray) vs. mass (A–C), estimated TEE (D and E) or mass/estimated TEE (F); see Fig. 1 for estimation equations. Shaded areas indicate 95% confidence regions for the OLS regression.