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...
Female chimpanzees exhibit exceptionally slow rates of reproduction and raise their offspring without direct paternal care. Therefore, their reproductive success depends critically on long-term access to high-quality food resources over a long lifespan. Chimpanzee communities contain multiple adult males, multiple adult females and their offspring. Because males are philopatric and jointly defend the community range while most females transfer to new communities before breeding, adult females are typically surrounded by unrelated competitors. Communities are fission-fusion societies in which individuals spend time alone or in fluid subgroups, whose size depends mostly on the abundance and distribution of food. To varying extents in different populations, females avoid direct competition by foraging alone or in small groups in distinct, but overlapping core areas within the community range to which they show high fidelity. Although rates of aggression are low, females compete for space and access to food. High rank correlates with high reproductive success, and high-ranking females win direct contests for food and gain preferential access to resource-rich sites. Females are aggressive to immigrant females and even kill the newborn infants of community members. The intensity of such aggression correlates with population density. These patterns are compared to those in other species, including humans.
In most primate societies, strong and enduring social bonds form preferentially among kin, who benefit from cooperation through direct and indirect fitness gains. Chimpanzees, Pan troglodytes, differ from most species by showing consistent female-biased dispersal and strict male philopatry. In most East African populations, females tend to forage alone in small core areas and were long thought to have weak social bonds of little biological significance. Recent work in some populations is challenging this view. However, challenges remain in quantifying the influence of shared space use on association patterns, and in identifying the drivers of partner preferences and social bonds. Here, we use the largest data set on wild chimpanzee behaviour currently available to assess potential determinants of female association patterns. We quantify pairwise similarities in ranging, dyadic association and grooming for 624 unique dyads over 38 years, including 17 adult female kin dyads. To search for social preferences that could not be explained by spatial overlap alone, we controlled for expected association based on pairwise kernel volume intersections of core areas. We found that association frequencies among females with above-average overlap correlated positively with grooming rates, suggesting that associations reflected social preferences in these dyads. Furthermore, when available, females preferred kin over nonkin partners for association and grooming, and variability was high among nonkin dyads. While variability in association above and below expected values was high, on average, nonkin associated more frequently if they had immature male offspring, while having female offspring had the opposite effect. Dominance rank, an important determinant of reproductive success at Gombe, influenced associations primarily for low-ranking females, who associated preferentially with each other. Our findings support the hypothesis that female chimpanzees form well-differentiated social relationships that are of potential adaptive value to females and their offspring.
Female space use can have important fitness consequences, which are likely due to differential access to food resources. Many studies have explored spatial competition in solitary species, but little is known about how individuals in social species compete over shared space. In this study, we investigate spatial patterns of aggression among female East African chimpanzees, Pan troglodytes schweinfurthii. This species provides an excellent opportunity to study spatial competition since (1) female chimpanzees occupy overlapping core areas (small areas of the community range in which individuals concentrate their space use) and (2) female core area quality is correlated with reproductive success, suggesting that females compete over long-term access to core areas. Here, we examine how female aggression towards other females varies inside and outside individual female core areas during a 14-year period at Gombe National Park, Tanzania. Overall, females showed higher rates of aggression inside than outside their own core areas. This pattern was driven by spatial variation in aggression in nonfeeding contexts. While food-related aggression did not vary spatially, females were more aggressive in nonfeeding contexts inside their core areas than they were outside their core areas. These results suggest that female chimpanzees follow a mixed strategy in which they compete for long-term access to resources in their core areas as well as for immediate access to food throughout the community range.
While natural observations show apes use grooming and play as social currency, no experimental manipulations have been carried out to measure the effects of these behaviours on relationship formation in apes. While previous experiments have demonstrated apes quickly learn the identity of individuals who will provide food in a variety of cooperative and non-cooperative situations, no experiment has ever examined how grooming and play might shape the preferences of apes for different individuals. We gave a group bonobos () and chimpanzees () a choice between an unfamiliar human who had recently groomed or played with them and one who had not. Both species showed a preference for the unfamiliar human that had interacted with them over the one who did not. The effect was largely driven by the males of both species while interacting with females showed little effect on their preferences for unfamiliar humans. Subjects showed this preference even though they only had social interactions with one of the unfamiliar humans for a few minutes before each trial and their choices were not rewarded with food differentially. Our results support the long held idea that grooming and play act as a form of social currency in great apes (and likely many other species) that can rapidly shape social relationships, particularly between unfamiliar individuals.
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