Systematic mapping of developmental milestones in wild chimpanzees

ostnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens ), facilitating the acquisition of key motor, communication and social skills that can maximise fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one‐species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes ), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter‐individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d’Ivoire. Gross motor traits emerged at a mean of four months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter‐individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development

The male and female perspective in the link between male infant care and mating behaviour in Barbary macaques

Infant care from adult males is unexpected in species with high paternity uncertainty. Still, males of several polygynandrous primates engage in frequent affiliative interactions with infants. Two non‐exclusive hypotheses link male infant care to male mating strategies. The paternal investment hypothesis views infant care as a male strategy to maximize the survival of sired offspring, while the mating effort hypothesis predicts that females reward males who cared for their infant by preferably mating with them. Both hypotheses predict a positive relationship between infant care and matings with a particular female. However, the paternal investment hypothesis predicts that increased matings come before infant care whereas the mating effort hypothesis predicts that infant care precedes an increase in matings. Both hypotheses are usually tested from the perspective of the proportion of matings and care that individual females engage in and receive, rather than from the perspective of the care and mating behaviour of individual males. We tested the relationships between care and mating from both female and male perspectives in Barbary macaques. Mating predicted subsequent care and care predicted subsequent mating when viewed from the male but not the female perspective. Males mainly cared for infants of their main mating partners, but infants were not mainly cared for by their likely father. Males mated more with the mothers of their favourite infants, but females did not mate more with the main caretakers of their infants. We suggest that females do not choose their mating partners based on previous infant care, increasing paternity confusion. Males might try to increase paternal investment by distributing the care according to their own instead of female mating history. Further, males pursue females for mating opportunities based on previous care

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus)

Background: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth. In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear. The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. Results: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. Conclusion: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The ‘interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the ‘social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability

Maternal effects on the development of vocal communication in wild chimpanzees

Early-life experiences, such as maternal care received, influence adult social integration and survival. We examine what changes to social behavior through ontogeny lead to these lifelong effects, particularly whether early-life maternal environment impacts the development of social communication. Chimpanzees experience prolonged social communication development. Focusing on a central communicative trait, the "pant-hoot" contact call used to solicit social engagement, we collected cross-sectional data on wild chimpanzees (52 immatures and 36 mothers). We assessed early-life socioecological impacts on pant-hoot rates across development, specifically: mothers' gregariousness, age, pant-hoot rates and dominance rank, maternal loss, and food availability, controlling for current maternal effects. We found that early-life maternal gregariousness correlated positively with offspring pant-hoot rates, while maternal loss led to reduced pant-hoot rates across development. Males had steeper developmental trajectories in pant-hoot rates than females. We demonstrate the impact of maternal effects on developmental trajectories of a rarely investigated social trait, vocal production

Patterns of urinary cortisol levels during ontogeny appear population specifi c rather than species specifi c in wild chimpanzees and bonobos

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus)

Background In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth. In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear. The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. Results We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. Conclusion Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.Peer Reviewe