Wild chimpanzees exhibit humanlike aging of glucocorticoid regulation.

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.

Prenatal stress accelerates offspring growth to compensate for reduced maternal investment across mammals.

Across mammals, prenatal maternal stress (PREMS) affects many aspects of offspring development, including offspring growth. However, how PREMS translates to offspring growth is inconsistent, even within species. To explain the full range of reported effects of prenatal adversity on offspring growth, we propose an integrative hypothesis: developmental constraints and a counteracting adaptive growth plasticity work in opposition to drive PREMS effects on growth. Mothers experiencing adversity reduce maternal investment leading to stunted growth (developmental constraints). Concomitantly, the pace of offspring life history is recalibrated to partly compensate for these developmental constraints (adaptive growth plasticity). Moreover, the relative importance of each process changes across ontogeny with increasing offspring independence. Thus, offspring exposed to PREMS may grow at the same rate as controls during gestation and lactation, but faster after weaning when direct maternal investment has ceased. We tested these predictions with a comparative analysis on the outcomes of 719 studies across 21 mammal species. First, the observed growth changes in response to PREMS varied across offspring developmental periods as predicted. We argue that the observed growth acceleration after weaning is not "catch-up growth," because offspring that were small for age grew slower. Second, only PREMS exposure early during gestation produced adaptive growth plasticity. Our results suggest that PREMS effects benefit the mother's future reproduction and at the same time accelerate offspring growth and possibly maturation and reproductive rate. In this sense, PREMS effects on offspring growth allow mother and offspring to make the best of a bad start.

Prenatal stress effects in a wild, long-lived primate: predictive adaptive responses in an unpredictable environment.

Prenatal maternal stress affects offspring phenotype in numerous species including humans, but it is debated whether these effects are evolutionarily adaptive. Relating stress to adverse conditions, current explanations invoke either short-term developmental constraints on offspring phenotype resulting in decelerated growth to avoid starvation, or long-term predictive adaptive responses (PARs) resulting in accelerated growth and reproduction in response to reduced life expectancies. Two PAR subtypes were proposed, acting either on predicted internal somatic states or predicted external environmental conditions, but because both affect phenotypes similarly, they are largely indistinguishable. Only external (not internal) PARs rely on high environmental stability particularly in long-lived species. We report on a crucial test case in a wild long-lived mammal, the Assamese macaque (Macaca assamensis), which evolved and lives in an unpredictable environment where external PARs are probably not advantageous. We quantified food availability, growth, motor skills, maternal caretaking style and maternal physiological stress from faecal glucocorticoid measures. Prenatal maternal stress was negatively correlated to prenatal food availability and led to accelerated offspring growth accompanied by decelerated motor skill acquisition and reduced immune function. These results support the 'internal PAR' theory, which stresses the role of stable adverse internal somatic states rather than stable external environments.

Transition to siblinghood causes a substantial and long-lasting increase in urinary cortisol levels in wild bonobos.

In animals with slow ontogeny and long-term maternal investment, immatures are likely to experience the birth of a younger sibling before reaching maturity. In these species, the birth of a sibling marks a major event in an offspring's early life as the older siblings experience a decrease in maternal support. The transition to siblinghood (TTS) is often considered to be stressful for the older offspring, but physiological evidence is lacking. To explore the TTS in wild bonobos, we investigated physiological changes in urinary cortisol (stress response), neopterin (cell-mediated immunity), and total triiodothyronine (T3, metabolic rate), as well as changes in behaviors that reflect the mother-offspring relationship. Following a sibling's birth, urinary cortisol levels of the older offspring increased fivefold, independent of their age, and remained elevated for 7 months. The cortisol level increase was associated with declining neopterin levels; however, T3 levels and behavioral measures did not change. Our results indicate that the TTS is accompanied by elevated cortisol levels and that this change does not coincide with nutritional weaning and attainment of physical independence. Our results suggest that bonobos and humans experience TTS in similar ways and that this developmental event may have emerged in the last common ancestor.

Age-dependent change of coalitionary strategy in male Barbary macaques.

Inter- and intra-specific variation in the propensity to form coalitions has been explained by variation in the availability of suitable partners, distribution of fighting ability, coalition profitability, and costs of coordination. Male coalition formation can be an alternative reproductive strategy to one-on-one competition to maximize male reproductive success. Here we focus on age as a state variable to explain within-group variation in individual propensity to form coalitions against other group members. We specifically test the prediction that males conditionally switch from a solo strategy for achievement of high mating success to a cooperative strategy after reaching post-prime age in male Barbary macaques (Macaca sylvanus). We combined new observations with data collected in 2006 and 2008 on the same individuals from one captive group living in semi-natural conditions at Affenberg Salem, Germany, and found that in all years males between 5 and 13 years formed significantly fewer coalitions than males 14 years and older (post-prime). More importantly, we found those males that aged into the post-prime phase to have switched their reproductive strategy and to form significantly more coalitions in 2014 compared to 2008. These first longitudinal data together with earlier cross-sectional analyses in this and other primate species suggest that group-level measures of coalition propensity may be strongly affected by the age composition of groups and that male coalition formation can be a conditional reproductive strategy.

Patterns and Consequences of Male-Infant Relationships in Wild Assamese Macaques (Macaca assamensis).

Male care for offspring is unexpected in polygynandrous mammals. Evidence from nonhuman primates, however, indicates not only the existence of stable male-immature associations in multimale-multifemale groups, but also male care in the form of protection from infanticidal attacks and conspecific harassment. Here, we investigate the relationship characteristics, dynamics, and consequences of male-immature associations in wild Assamese macaques, Macaca assamensis, at Phu Khieo Wildlife Sanctuary, Thailand, to inform hypotheses of their evolutionary origins. Female Assamese macaques reproduce seasonally and do not signal ovulation, resulting in low mating and paternity skew. However, male-immature associations are predicted by paternity, and male behavior potentially reflects paternal effort. We present focal animal data on 12 immatures followed from birth beyond weaning into their juvenile life (1188 focal hours). The distribution of composite sociality indices suggests that male-immature relationships were highly differentiated. Association patterns and the degree of differentiation remained stable from 6 mo well into the juvenile phase, suggesting that male protection extends beyond the phase of high infanticide risk. Based on Hinde indices, immatures were responsible for maintaining the relationships. The likelihood that an infant was associated with its preferred male increased if the mother was absent and if other males were present in proximity, suggesting that immatures sought protection. The presence of the preferred male did not decrease the rate of mild aggression immatures received from group members, but the stronger the relationship between an immature and a male, the more often it received agonistic support from him. Future studies will have to assess whether this agonistic support translates into improved fitness and represents true paternal care.

Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off.

The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences. Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits. Prominent theories propose that locomotor play is (i) low cost, using surplus energy remaining after growth and maintenance, and (ii) beneficial because it trains motor skills. However, both theories are largely untested. Studying wild Assamese macaques, we combined behavioral observations of locomotor play and motor skill acquisition with quantitative measures of natural food availability and individual growth rates measured noninvasively via photogrammetry. Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth. Even under moderate natural energy restriction, investment in locomotor play accounted for up to 50% of variance in growth, which strongly contradicts the current theory that locomotor play only uses surplus energy remaining after growth and maintenance. Male immatures played more, acquired motor skills faster, and grew less than female immatures, leading to persisting size differences until the age of female maturity. Hence, depending on skill requirements, investment in play can take ontogenetic priority over physical development unconstrained by costs of play with consequences for life history, which strongly highlights the ontogenetic and evolutionary importance of play.