Cortisol, a key product of the stress response, has critical influences on degenerative aging in humans. In turn, cortisol production is affected by senescence of the hypothalamic–pituitary–adrenal (HPA) axis, leading to progressive dysregulation and increased cortisol exposure. These processes have been studied extensively in industrialized settings, but few comparative data are available from humans and closely related species living in natural environments, where stressors are very different. Here, we examine age-related changes in urinary cortisol in a 20-y longitudinal study of wild chimpanzees (n = 59 adults) in the Kanyawara community of Kibale National Park, Uganda. We tested for three key features of HPA aging identified in many human studies: increased average levels, a blunted diurnal rhythm, and enhanced response to stressors. Using linear mixed models, we found that aging was associated with a blunting of the diurnal rhythm and a significant linear increase in cortisol, even after controlling for changes in dominance rank. These effects did not differ by sex. Aging did not increase sensitivity to energetic stress or social status. Female chimpanzees experienced their highest levels of cortisol during cycling (versus lactation), and this effect increased with age. Male chimpanzees experienced their highest levels when exposed to sexually attractive females, but this effect was diminished by age. Our results indicate that chimpanzees share some key features of HPA aging with humans. These findings suggest that impairments of HPA regulation are intrinsic to the aging process in hominids and are side effects neither of extended human life span nor of atypical environments.

Life history theory predicts a trade-off between offspring quality and quantity. Among large-bodied mammals, prolonged lactation and infant dependence suggest particularly strong potential for a qualityquantity trade-off to exist. Humans are one of the only such species to have been examined, providing mixed evidence under a peculiar set of circumstances, including extensive nutritional provisioning by nonmothers and extrasomatic wealth transmission. Here, we examine trade-offs between reproductive rate and one aspect of offspring quality (body size) in wild chimpanzees (Pan troglodytes schweinfurthii), a species with long periods of infant dependence and little direct provisioning. Juvenile lean body mass, estimated using urinary creatinine excretion, was positively associated with the interval to the next sibling's birth. These effects persisted into adolescence and were not moderated by maternal identity. Maternal depletion could not explain poor offspring growth, as older mothers had larger offspring, and low maternal energy balance during lactation predicted larger, not smaller, juvenile size. Instead, our data suggest that offspring growth suffers when mothers wean early to invest in new reproductive efforts. These findings indicate that chimpanzee mothers with the resources to do so prioritize production of new offspring over prolonged investment in current offspring.life history | growth | reproduction | primates | weaning P arents face a fundamental life-history trade-off between producing more offspring and investing in the quality of each progeny (1-4). This offspring quality-quantity trade-off, along with a trade-off between reproductive investment and parental survival, means that maximizing reproductive rates is often not the strategy that maximizes fitness (5-7). The quality-quantity trade-off has been empirically demonstrated in species that produce litters or clutches, where large litter size often leads to small offspring size, slow growth rates, and reduced survival, particularly under conditions of ecological stress (8-11). Comparative analyses also support a negative interspecific relationship between reproductive rate and offspring size (12, 13). The quality-quantity trade-off has rarely been examined in species for which single births are the norm, and for which reproductive rate is determined by the interval between successive births. Such species are important tests of the model, as a slow breeding strategy suggests a particularly potent trade-off between offspring investment and reproductive rate. Understanding how individuals negotiate this trade-off can provide important insights into the evolution of reproductive biology and behavior.Data on humans are valuable because humans invest intensively in offspring, yet have highly variable reproductive rates. Many studies find the predicted negative relationship between reproductive rates and offspring growth or health (14-18) or demonstrate fitness maximization at intermediate levels of fertility (19-21). For example, when a water tap was ...

While declining physical performance is an expected consequence of ageing, human clinical research has placed increasing emphasis on physical frailty as a predictor of death and disability in the elderly. We examined non-invasive measures approximating frailty in a richly sampled longitudinal dataset on wild chimpanzees. Using urinary creatinine to assess lean body mass, we found moderate but significant declines in physical condition with age in both sexes. While older chimpanzees spent less of their day in the trees and feeding, they did not alter activity budgets with respect to travel or resting. There was little evidence that declining lean body mass had negative consequences independent of age. Old chimpanzees with poor lean body mass rested more often but did not otherwise differ in activity. Males, but not females, in poor condition were more likely to exhibit respiratory illness. Poor muscle mass was associated acutely with death in males, but it did not predict future mortality in either sex. While there may be some reasons to suspect biological differences in the susceptibility to frailty in chimpanzees versus humans, our data are consistent with recent reports from humans that lean, physically active individuals can successfully combat frailty. This article is part of the theme issue ‘Evolution of the primate ageing process’.

The development of the adrenal cortex varies considerably across primates, being most conspicuous in humans, where a functional zona reticularis-the site of dehydroepiandrosterone-sulfate (DHEA/S) production-does not develop until middle childhood (5-8 years). Prior reports suggest that a human-like adrenarche, associated with a sharp prepubertal increase in DHEA/S, may only occur in the genus Pan. However, the timing and variability in adrenarche in chimpanzees remain poorly described, owing to the lack of longitudinal data, or data from wild populations. Here, we use urine samples from East African chimpanzees (Pan troglodytes schweinfurthii) collected over 20 years at Kanyawara in Kibale National Park, Uganda, to trace the developmental trajectories of DHEAS (n = 1,385 samples, 53 individuals) and cortisol (n = 12,726 samples, 68 individuals). We used generalized additive models (GAM) to investigate the relationship between age, sex, and hormone levels. Adrenarche began earlier in chimpanzees (~2-3 years) compared with what has been reported in humans (6-8 years) and, unlike humans, male and female chimpanzees did not differ significantly in the timing of adrenarche nor in DHEAS concentrations overall. Similar to what has been reported in humans, cortisol production decreased through early life, reaching a nadir around puberty (8-11 years), and a sex difference emerged with males exhibiting higher urinary cortisol levels compared with females by early adulthood (15-16 years). Our study establishes that wild chimpanzees exhibit a human-like pattern of cortisol production during development and corroborates prior reports from captive chimpanzees of a human-like adrenarche, accompanied by significant developmental increases in DHEAS. While the role of these developmental hormone shifts are as yet unclear, they have been implicated in stages of rapid behavioral development once thought unique to humans, especially in regard to explaining the divergence of female and male social behavior before pubertal increases in gonadal hormones.

Dental caries has been reported in a variety of primates, although it is still considered rare in wild populations. In this study, 11 catarrhine primate taxa (n = 339 individuals; 7946 teeth) were studied for the presence of caries. A differential diagnosis of lesions in interproximal regions of anterior teeth was undertaken, since they had been previously described as both carious and non‐carious in origin. Each permanent tooth was examined macroscopically, with severity and position of lesions recorded. Two specimens were examined further, using micro‐CT scans to assess demineralization. Differential diagnosis confirmed the cariogenic nature of interproximal cavities on anterior teeth (ICATs). Overall results show 3.3% of all teeth (i.e., anterior and posterior teeth combined) were carious (n = 262), with prevalence varying among species from 0% to >7% of teeth affected. Those with the highest prevalence of ICATs include Pan troglodytes verus (9.8% of anterior teeth), Gorilla gorilla gorilla (2.6%), Cercopithecus denti (22.4%), Presbytis femoralis (19.5%), and Cercopithecus mitis (18.3%). ICATs make up 87.9% of carious lesions on anterior teeth. These results likely reflect dietary and food processing differences among species, but also between the sexes (e.g., 9.3% of all female P. troglodytes verus teeth were carious vs. 1.8% in males). Processing cariogenic fruits and seeds with the anterior dentition (e.g., wadging) likely contributes to ICAT formation. Further research is needed in living primate populations to ascertain behavioral/dietary influences on caries occurrence. Given the presence of ICATs in frugivorous primates, their diagnosis in archaeological and paleontological specimens may shed light on diet and food processing behaviors in fossil primates.