Abstract
Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.
Highlights
Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure independent of body mass
In primates and other placental mammals, growth, maternal investment, and life expectancy are positively related to total daily energy expenditure (DEE)[4,6] but since most life history traits and brain size are connected to body mass, e.g.,1,7, looking for a correlated evolution between life history and energy expenditure necessitates to remove the effect of body mass
DEE data used here were collected from non-gestating, non-lactating adults, mainly reflecting basal energy requirements, physical activity, and physiological regulation for maintaining body homeostasis (Table 1). With this set of 18 human and nonhuman primate species, the phylogenetic generalized least square (PGLS) regression of DEE on species body mass (Fig. 1) conformed to the expected pattern: after Ln-Ln transformation, the slope of the regression line was 0.66, which corresponds to previous estimates and shows that the DEE per unit body mass is lower in larger species[2,18,19]
Summary
Brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. In primates and other placental mammals, growth, maternal investment, and life expectancy are positively related to total daily energy expenditure (DEE)[4,6] but since most life history traits and brain size are connected to body mass, e.g.,1,7, looking for a correlated evolution between life history and energy expenditure necessitates to remove the effect of body mass. A recent meta-analysis on eutherian mammals, including primates[2], found a positive relationship between daily energy expenditure and reproductive output (litter mass/interbirth interval) controlling for body mass but the link was weak due to the great variability of reproductive data and was not found for two other life history traits (growth and maximum lifespan). Contrary to our prediction that energy limitation in Madagascar selected for low energy expenditure strategies, we provide evidence that lemurs do not differ from other primates on average, but invest comparatively less energy for reproduction than for somatic maintenance
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