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Significance The metabolic costs of brain development are thought to explain the evolution of humans’ exceptionally slow and protracted childhood growth; however, the costs of the human brain during development are unknown. We used existing PET and MRI data to calculate brain glucose use from birth to adulthood. We find that the brain’s metabolic requirements peak in childhood, when it uses glucose at a rate equivalent to 66% of the body’s resting metabolism and 43% of the body’s daily energy requirement, and that brain glucose demand relates inversely to body growth from infancy to puberty. Our findings support the hypothesis that the unusually high costs of human brain development require a compensatory slowing of childhood body growth.

The mother-offspring relationship is paramount in most mammals and infant survival often depends on maternal investment. In species with prolonged periods of development or co-residence, mothers may continue to influence their offspring’s outcomes beyond nutritional independence with benefits biased towards the philopatric sex. Chimpanzees (Pan troglodytes) are long-lived mammals with a protracted period of immaturity during which offspring continue to travel with their mothers. In contrast to most mammals, chimpanzees are also typically male philopatric. Here, we use over 50 years of demographic data from two communities in Gombe National Park, Tanzania, to examine the survival and longevity of both male and female chimpanzees that experienced maternal loss during three different age categories. Males who were orphaned between the ages of 0–4.99 years, 5–9.99 years, and 10–14.99 years all faced significantly lower survival than non-orphans and died earlier than expected. Females faced similarly reduced survival probabilities when orphaned between 0–4.99 and 5–9.99 years of age; however, females who experienced maternal loss between 10 and 14.99 years of age were no more likely to die than non-orphans. Females orphaned in this later age class also lived significantly longer beyond maternal loss than their male counterparts. As observed in other mammals, philopatric male chimpanzees may continue to benefit from their mother’s ecological knowledge, whereas maternal influence on female offspring likely fades as they prepare to emigrate. These results emphasize how maternal influence on offspring outcomes can extend well beyond weaning, particularly for the philopatric sex.

We describe the individual and combined use of vocalizations and gestures in wild chimpanzees. The rate of gesturing peaked in infancy and, with the exception of the alpha male, decreased again in older age groups, while vocal signals showed the opposite pattern. Although gesture-vocal combinations were relatively rare, they were consistently found in all age groups, especially during affiliative and agonistic interactions. Within behavioural contexts rank (excluding alpha-rank) had no effect on the rate of male chimpanzees' use of vocal or gestural signals and only a small effect on their use of combination signals. The alpha male was an outlier, however, both as a prolific user of gestures and recipient of high levels of vocal and gesture-vocal signals. Persistence in signal use varied with signal type: chimpanzees persisted in use of gestures and gesture-vocal combinations after failure, but where their vocal signals failed they tended to add gestural signals to produce gesture-vocal combinations. Overall, chimpanzees employed signals with a sensitivity to the public/private nature of information, by adjusting their use of signal types according to social context and by taking into account potential out-of-sight audiences. We discuss these findings in relation to the various socio-ecological challenges that chimpanzees are exposed to in their natural forest habitats and the current discussion of multimodal communication in great apes.

Human language has no parallel elsewhere in the animal kingdom. It is unique not only for its structural complexity but also for its inextricable interface with core cognitive capacities such as object representation, object categorization and abstract rule learning. Here, we (i) review recent evidence documenting how (and how early) language interacts with these core cognitive capacities in the mind of the human infant, and (ii) consider whether this link exists in non-human great apes—our closest genealogical cousins. Research with human infants demonstrates that well before they begin to speak, infants have already forged a link between language and core cognitive capacities. Evident by just three months of age, this language–cognition link unfolds in a rich developmental cascade, with each advance providing the foundation for subsequent, more precise and more powerful links. This link supports our species' capacity to represent and convey abstract concepts and to communicate beyond the immediate here and now. By contrast, although the communication systems of great apes are sophisticated in their own right, there is no conclusive evidence that apes establish reference, convey information declaratively or pass down communicative devices via cultural transmission. Thus, the evidence currently available reinforces the uniqueness of human language and the power of its interface to cognition. This article is part of the theme issue ‘What can animal communication teach us about human language?’

Parental care strategies are adaptations shaped by evolutionary pressures to maximize offspring survival while balancing current and future reproductive investment. Maternal care styles, which are consistent patterns of behavior that vary among individuals, have been well-documented in catarrhines but remain poorly understood in platyrrhines. Furthermore, while previous studies have documented that maternal behaviors change as infants develop, whether individual maternal styles remain consistent or shift across infant developmental stages remains largely unexplored. This represents a critical gap, because understanding the interaction between maternal styles and infant age could reveal whether mothers maintain fixed behavioral phenotypes or demonstrate flexible responses to changing developmental needs. We investigated whether wild mantled howler monkeys (Alouatta palliata) show distinct maternal care styles that change across infant development. Using an age-specific analytical approach, we examined whether maternal behavior is organized into distinct styles during each of early, middle, and late infant development. We observed 16 mother-infant dyads in four groups at three sites in Los Tuxtlas, Mexico, collecting 743 hours of focal observations over 2 years. Using robust principal component analysis and bootstrap-validated cluster analysis, we identified three distinct maternal styles during early infancy (Minimal-investment, High investment, and Proximity-focused), three styles during middle infancy (Minimal-investment, High-support, and Mixed-investment), and two styles during late infancy (Minimal-investment and Selective-support). We found minimal consistency in individual maternal styles across infant development stages, with infant age significantly explaining behavioral variance whereas maternal identity did not. Our results offer preliminary evidence that mantled howler monkey mothers strategically adjust care patterns in response to infant developmental needs rather than maintaining consistent individual styles. If such dynamic adjustment allows for the successful balancing of the competing demands of ensuring current offspring survival and maintaining capacity for future reproduction, our results contribute to the understanding of the evolution of maternal investment strategies in primates.

Despite the strong link between childhood maltreatment and psychopathology, the underlying neurodevelopmental mechanisms are poorly understood and difficult to disentangle from heritable and prenatal factors. This study used a translational macaque model of infant maltreatment in which the adverse experience occurs in the first months of life, during intense maturation of amygdala circuits important for stress and emotional regulation. Thus, we examined the developmental impact of maltreatment on amygdala functional connectivity (FC) longitudinally, from infancy through the juvenile period. Using resting state functional magnetic resonance imaging (MRI) we performed amygdala–prefrontal cortex (PFC) region-of-interest and exploratory whole-brain amygdala FC analyses. The latter showed (a) developmental increases in amygdala FC with many regions, likely supporting increased processing of socioemotional-relevant stimuli with age; and (b) maltreatment effects on amygdala coupling with arousal and stress brain regions (locus coeruleus, laterodorsal tegmental area) that emerged with age. Maltreated juveniles showed weaker FC than controls, which was negatively associated with infant hair cortisol concentrations. Findings from the region-of-interest analysis also showed weaker amygdala FC with PFC regions in maltreated animals than controls since infancy, whereas bilateral amygdala FC was stronger in maltreated animals. These effects on amygdala FC development may underlie the poor behavioral outcomes associated with this adverse experience.

Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition--a shift in socio-emotional preferences—also occurs in non-human primates. Specifically, we experimentally measured socioemotional processing in a large population of rhesus macaques (Macaca mulatto) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socio-emotional stimuli, to a positivity bias at older ages. We first assessed monkeys' (n = 337) responses to negative socio-emotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys' (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Dehydroepiandrosterone-sulfate (DHEAS) is the most abundant steroid in humans and some nonhuman primates. This adrenal androgen contributes to immune enhancement, neuroprotection, and reproduction. In humans and apes, DHEAS levels increase before puberty, a phenomenon called adrenarche. However, a postnatal increase in the levels of these hormones is not apparent in cercopithecoids. In marmosets, DHEAS is only synthesized from female adrenal glands, if their ovarian function is compromised. However, DHEAS is poorly investigated among other platyrrhines. Our main objective was to test the influence of sex and age on fecal and serum DHEAS levels in black-and-gold howler monkeys ( Alouatta caraya ) under human care. We measured DHEAS levels in feces from 16 females and 21 males aged between 6 months and 26 years old and in serum from 27 of those animals using a commercial enzyme immunoassay kit. We found high levels of serum DHEAS in adult females, and DHEAS levels in fecal and serum samples were strongly and positively correlated. Fecal DHEAS levels showed a quadratic relationship with age, increasing from infancy to adulthood, then declining in older adults. There was no significant effect of sex, although females had a greater range than males. The postnatal increase in DHEAS levels in howler monkeys is like that of apes and humans, while the large variation in DHEAS levels among adult females suggests that, as in marmosets, DHEAS may be important for female howler monkey reproduction. This pattern highlights the importance of comparative studies to investigate the biological function of DHEAS in evolution. Graphical Abstract

Despite the evident socioecological importance, knowledge of olfactory communication in Neotropical primates is in its infancy. Thus, to aid our understanding, we report on and describe olfactory communication behavior in Endangered Coimbra-Filho’s titi monkey (Callicebus coimbrai) in two Atlantic Forest fragments in northeastern Brazil. We discuss our data using intragroup (communication and sexual attraction) and intergroup (territoriality) contexts. We systematically observed two titi monkey groups, one at Fazenda Trapsa (21 mo: 1513 h) and another at Mata do Junco (11 mo: 683 h). We recorded data on olfactory signals via all-occurrence sampling. We registered 14 olfaction-linked events in which the titi monkey pressed the right hand against the gular and sternal body regions and then wiped the palm repeatedly on the nearby branch. Adult males performed 11 events, whereas adult females performed the remaining 3. Most events associated with intragroup encounters had a sexual context. The events related to intergroup encounters appeared to be related to territorial defense. Our study provides the first evidence that Coimbra-Filho’s titi monkey uses olfactory communication for both intragroup and intergroup communication. Dominance, mate attraction, and territorial defense functions shown by Coimbra-Filho titi monkeys in their olfactory behaviors provide new insights into the socioecology of Callicebusand potential themes for future research.