Rachna B. Reddy’s research while affiliated with Harvard University and other places

Life history theory addresses how organisms balance development and reproduction. Mammals usually invest considerable energy into growth in infancy, and they do so incrementally less until reaching adult body size, when they shift energy to reproduction. Humans are unusual in having a long adolescence when energy is invested in both reproduction and growth, including rapid skeletal growth around puberty. Although many primates, especially in captivity, experience accelerated growth in mass around puberty, it remains unclear whether this represents skeletal growth. Without data on skeletal growth in nonhuman primates, anthropologists have often assumed the adolescent growth spurt is uniquely human, and hypotheses for its evolution have focused on other uniquely human traits. The lack of data is largely due to methodological difficulties of assessing skeletal growth in wild primates. Here, we use two urinary markers of bone turnover-osteocalcin and collagen-to study skeletal growth in a large, cross-sectional sample of wild chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda. For both bone turnover markers, we found a nonlinear effect of age, which was largely driven by males. For male chimpanzees, values for osteocalcin and collagen peaked at age 9.4 years and 10.8 years, respectively, which corresponds to early and middle adolescence. Notably, collagen values increased from 4.5 to 9 years, suggesting faster growth during early adolescence compared to late infancy. Biomarker levels plateaued at 20 years in both sexes, suggesting skeletal growth continues until then. Additional data, notably on females and infants of both sexes, are needed, as are longitudinal samples. However, our cross-sectional analysis suggests an adolescent growth spurt in the skeleton of chimpanzees, especially for males. Biologists should avoid claiming that the adolescent growth spurt is uniquely human, and hypotheses for the patterns of human growth should consider variation in our primate relatives.

Two capacities considered foundational in human cooperation are prosocial motivation and goal-reading abilities that enable helping. Children exhibit both proclivities by age 2 in interactions with other humans, but interactions with nonhuman species on whom we have been interdependent for millennia are unstudied. We tested the hypothesis that children’s goal-reading and prosocial propensities extend to other animals. We predicted children would help pet dogs access objects that dogs attempted to reach but could not reach themselves. We studied 97 children between 2 and 3 years of age living in a small mid-western US city, 44 of whom had dogs as household pets. In a quasi-naturalistic setting, we introduced children to 1 of 3 friendly pet dogs who remained within a small, porous enclosure while a treat or toy was placed outside it. Dogs reacted naturally, either showing interest in accessing the item (e.g., pawing, begging) or ignoring it. Measures of dog and child behavior during sessions were coded blindly with high reliability. Children provided dogs with out-of-reach items twice as often when dogs showed interest rather than ignored items, indicating sensitivity to the dog’s goals. Additionally, children were more generally likely to provide dogs with items if children lived with pet dogs, if dogs were more lively and engaged rather than subdued and if the item was a treat rather than a toy. These findings lend support to our hypothesis that children’s early-developing proclivities for goal-reading and prosociality extend beyond humans to other animals.

In humans, puberty initiates a period of rapid and formative neurobehavioral development. Brain and behavior changes during this maturational window contribute to opportunities for social learning. Here we provide new insights into adolescence as a unique period of social learning and development by describing field studies of our closest living relatives, chimpanzees. Like humans, chimpanzees have a multiyear juvenile life stage between weaning and puberty onset followed by a multiyear adolescent life stage after pubertal onset but prior to socially-recognized adulthood. As they develop increasing autonomy from caregivers, adolescent chimpanzees explore and develop many different types of social relationships with a wide range of individuals in a highly flexible social environment. We describe how adolescent social motivations and experiences differ from those of juveniles and adults and expose adolescents to high levels of uncertainty, risk, and vulnerability, as well as opportunities for adaptive social learning. We discuss how these adolescent learning experiences may be shaped by early life and in turn shape varied adult social outcomes. We outline how future chimpanzee field research can contribute in new ways to a more integrative interdisciplinary understanding of adolescence as a developmental window of adaptive social learning and resilience.

Viral infection is a major cause of ill health in wild chimpanzees (Pan troglodytes), but most evidence to date has come from conspicuous disease outbreaks with high morbidity and mortality. To examine the relationship between viral infection and ill health during periods not associated with disease outbreaks, we conducted a longitudinal study of wild eastern chimpanzees (P. t. schweinfurthii) in the Kanyawara and Ngogo communities of Kibale National Park, Uganda. We collected standardized, observational health data for 4 years and then used metagenomics to characterize gastrointestinal viromes (i.e., all viruses recovered from fecal samples) in individual chimpanzees before and during episodes of clinical disease. We restricted our analyses to viruses thought to infect mammals or primarily associated with mammals, discarding viruses associated with nonmammalian hosts. We found 18 viruses (nine of which were previously identified in this population) from at least five viral families. Viral richness (number of viruses per sample) did not vary by health status. By contrast, total viral load (normalized proportion of sequences mapping to viruses) was significantly higher in ill individuals compared with healthy individuals. Furthermore, when ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher infection rates with certain viruses and higher total viral loads as they aged. Post-hoc analyses, including the use of a machine-learning classification method, indicated that one virus, salivirus (Picornaviridae), was the main contributor to health-related and community-level variation in viral loads. Another virus, chimpanzee stool-associated virus (chisavirus; unclassified Picornavirales), was associated with ill health at Ngogo but not at Kanyawara. Chisavirus, chimpanzee adenovirus (Adenoviridae), and bufavirus (Parvoviridae) were also associated with increased age in males. Associations with sex and age are consistent with the hypothesis that nonlethal viral infections cumulatively reflect or contribute to senescence in long-lived species such as chimpanzees. Research Highlights • Some viruses of wild primates are relatively benign but may be useful as biomarkers of physiology and health. • We used metagenomic methods to characterize viral communities in feces of wild chimpanzees in two long-term study communities (Kanyawara and Ngogo) in Kibale National Park, Uganda. • Chimpanzees exhibited higher viral loads (normalized abundances of viral genetic sequences) when they were ill than when those same individuals were previously healthy. • When ill, Kanyawara chimpanzees exhibited higher viral loads than Ngogo chimpanzees, and males, but not females, exhibited higher viral loads as they aged.

Caring for others is a key feature of human behavior. Mothers, fathers, siblings, grandparents, and other group members provide care in the form of provisioning, protection, and first aid. To what extent is other-regarding behavior present in our primate relatives? Here we describe an unusual incident of other-regarding behavior toward an injured juvenile female chimpanzee (Pan troglodytes schweinfurthii) at Ngogo in Kibale National Park, Uganda. After the juvenile received a mild head wound from an adult female, several adolescent and juvenile chimpanzees gathered to touch, lick, and peer at the wound. One adolescent male wiped a leaf across the cut. Another adolescent male later groomed the injured female and briefly carried her. Across a 5-year period, we observed only three other instances of other-directed wound care in chimpanzees, occurring in 4% (4/100) of cases in which we observed individuals with fresh wounds, and 57 other instances of allomaternal carrying. Despite the infrequency of such behaviors, our study adds another chimpanzee field site to the list of those where other-directed wound care has been observed. Observations from wild chimpanzees provide insight into empathy and may inform our understanding of the evolution of other-regarding behavior in humans.

Many animals engage in sociosexual behaviour, including that between same-sex pairs. Bonobos ( Pan paniscus ) are famous for their sociosexual behaviour, but chimpanzees ( Pan troglodytes ) apparently do not engage in sociosexual behaviour frequently. However, sociosexual behaviour in chimpanzees may have been overlooked. We observed 584 instances of sociosexual behaviour in chimpanzees at Ngogo, Kibale National Park, Uganda during three years of study. All ages and sexes engaged in sociosexual behaviour, which included mounting, touching of genitals, and pressing genitals together. Most sociosexual behaviour was between adult males. Sociosexual behaviour was often during tense contexts, such as subgroup reunions and during territorial behaviour. Among males, grooming and dominance rank relationships do not explain patterns of sociosexual behaviour. Although sociosexual behaviour may be less frequent in chimpanzees than in bonobos, and bonobos remain distinct in their genito-genital rubbing, our findings suggest that sociosexual behaviour is a regular part of chimpanzee behaviour.

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.

Mothers provide indispensable care for infants in many mammalian species. In some long-lived species, the maternal-offspring bond persists after infancy with mothers continuing to provide resources and social support to their adult progeny. Maternal presence is associated with fitness benefits through adolescence for male chimpanzees despite the fact that mature males dominate females and form their strongest bonds with other males. How mothers support grown sons is unknown, because few studies have examined developmental shifts in mother-son relationships during adolescence and adulthood. We investigated social interactions between 29 adolescent (9–15 years) and young adult male (16–20 years) chimpanzees and their mothers at Ngogo in Kibale National Park, Uganda, over 3 years. All males under 12 years old had their mother as their top grooming and proximity partner, as did one-third of the young adult males. As males grew older, the amount of time they associated with, maintained proximity to, groomed with, and kept track of their mothers while traveling decreased. When males were together in the same party as their mothers, however, young adult males affiliated with their mothers as frequently as did adolescent males, with sons initiating the majority of these interactions. In contrast to adult sons, however, adolescent sons became distressed when separated from mothers and relied on their mothers for agonistic support and reassurance after conflicts. These findings indicate that the chimpanzee maternal-offspring bond continues but changes through adolescence and adulthood, with mothers remaining occasional social companions for most adult sons and frequent companions for some. Significance statement Mammalian mothers protect and provision their infants, and in some species, mothers provide social support for their adult offspring. The importance of mothers in the lives of adult sons is clear in humans and in one of our closest relatives, bonobos. Here we show mothers are also important social partners for sons throughout adolescence and into young adulthood in chimpanzees. Despite prevailing knowledge that adult males are key alliance partners for male chimpanzees, we demonstrate that male chimpanzees maintain social bonds with their mothers into adulthood. We also suggest that social bonds reflect not only the total time spent together, but what animals do during those times, as many young adults rarely groomed their mothers, but at times when they were in the same subgroup with her, they did so frequently. Future research will assess the physiological, psychological, and reproductive benefits of such mother-son bonds.