Age-related reproductive effort in male chimpanzees: terminal investment or alternative tactics?

Because senescence impairs the ability of older males to compete successfully for mates, male reproductive strategies are expected to change with age. The terminal investment hypothesis proposes that older males, who could die soon, should take greater risks to obtain mating opportunities. Another possibility is that older males avoid such risks, adopting alternative reproductive tactics, such as increased affiliation with females, increased reliance on coalitions or sexual coercion to continue to compete with younger animals. We tested these hypotheses in wild chimpanzees, Pan troglodytes schweinfurthii, of the Kanyawara community, Kibale National Park, Uganda, where old males sire offspring at relatively high rates. Our data set included >40 000 incidents of male aggression and >5800 copulations observed between 2005 and 2017. We found that, even as their dominance status declined, old males maintained relatively high copulation rates, especially with established mothers. There was no evidence for terminal investment in response to ageing. Males became generally less aggressive as they aged. Neither did old males form affiliative bonds with females, nor use sexual coercion more frequently, as alternative reproductive tactics. Old males did, however, participate in coalitionary aggression at higher rates than young males and increased the proportion of their aggression that was coalitionary over time. Coalitions were positively associated with mating success, particularly for low- and middle-ranking males. These results support the hypothesis that ageing male chimpanzees use coalitions as an alternative reproductive tactic. The lack of evidence for terminal investment in response to ageing appears to reflect a broader mammalian pattern in which males who rely on fighting to secure mating opportunities avoid excessive risk taking as their formidability wanes.

Ecological variation in adult social play reveals a hidden cost of motherhood for wild chimpanzees.

Though common among humans, social play by adults is an uncommon occurrence in most animals, even between parents and offspring.1,2,3 The most common explanation for why adult play is so rare is that its function and benefits are largely limited to development, so that social play has little value later in life.3,4,5,6 Here, we draw from 10 years of behavioral data collected by the Kibale Chimpanzee Project to consider an alternative hypothesis: that despite its benefits, adult play in non-humans is ecologically constrained by energy shortage or time limitations. We further hypothesized that, since they may be the only available partners for their young offspring, mother chimpanzees pay greater costs of play than other adults. Our analysis of nearly 4,000 adult play bouts revealed that adult chimpanzees played both among themselves and with immature partners. Social play was infrequent when diet quality was low but increased with the proportion of high-quality fruits in the diet. This suggests that adults engage in play facultatively when they have more energy and/or time to do so. However, when diet quality was low and most adult play fell to near zero, play persisted between mothers and offspring. Increased use of play by adult chimpanzees during periods of resource abundance suggests that play retains value as a social currency beyond development but that its costs constrain its use. At the same time, when ecological conditions constrain opportunities for young to play, play by mothers fills a critical role to promote healthy offspring development.

Language likely promoted peace before 100,000 ya.

Based on evidence of selection against alpha-male behavior in the earliest Homo sapiens, I suggest that by 300,000 ya (years ago) language would have been sufficiently sophisticated to contribute to peacemaking between groups. Language also influenced the social landscape of peace and war, and groups' ability to form coalitions.

Norm violations and punishments across human societies.

Punishments for norm violations are hypothesised to be a crucial component of the maintenance of cooperation in humans but are rarely studied from a comparative perspective. We investigated the degree to which punishment systems were correlated with socioecology and cultural history. We took data from the Standard Cross-Cultural Sample database and coded ethnographic documents from a sample of 131 largely non-industrial societies. We recorded whether punishment for norm violations concerned adultery, religion, food, rape or war cowardice and whether sanctions were reputational, physical, material or execution. We used Bayesian phylogenetic regression modelling to test for culture-level covariation. We found little evidence of phylogenetic signals in evidence for punishment types, suggesting that punishment systems change relatively quickly over cultural evolutionary history. We found evidence that reputational punishment was associated with egalitarianism and the absence of food storage; material punishment was associated with the presence of food storage; physical punishment was moderately associated with greater dependence on hunting; and execution punishment was moderately associated with social stratification. Taken together, our results suggest that the role and kind of punishment vary both by the severity of the norm violation, but also by the specific socio-economic system of the society.

Observational approaches to chimpanzee behavior in an African sanctuary: Implications for research, welfare, and capacity-building.

Research in African ape sanctuaries has emerged as an important context for our understanding of comparative cognition and behavior. While much of this work has focused on experimental studies of cognition, these animals semi-free-range in forest habitats and therefore can also provide important information about the behavior of primates in socioecologically-relevant naturalistic contexts. In this "New Approaches" article, we describe a project where we implemented a synthetic program of observational data collection at Ngamba Island Chimpanzee Sanctuary in Uganda, directly modeled after long-term data collection protocols at the Kibale Chimpanzee Project in Uganda, a wild chimpanzee field site. The foundation for this project was a strong partnership between sanctuary staff, field site staff, and external researchers. We describe how we developed a data-collection protocol through discussion and collaboration among these groups, and trained sanctuary caregivers to collect novel observational data using these protocols. We use these data as a case study to examine: (1) how behavioral observations in sanctuaries can inform primate welfare and care practices, such as by understanding aggression within the group; (2) how matched observational protocols across sites can inform our understanding of primate behavior across different contexts, including sex differences in social relationships; and (3) how more robust collaborations between foreign researchers and local partners can support capacity-building in primate range countries, along with mentoring and training students more broadly.

Associations between faecal chemical pollutants and hormones in primates inhabiting Kibale National Park, Uganda.

While anthropogenic pollutants are known to be a threat to primates, our understanding of exposure to pollutants in situ and their sub-lethal effects is still limited. We used non-invasive biomonitoring to examine associations between faecal concentrations of 97 chemical pollutants and faecal hormone metabolites of cortisol and oestradiol in four primate species inhabiting Kibale National Park, Uganda (chimpanzees-Pan troglodytes, olive baboons-Papio anubis, red colobus-Piliocolobus tephrosceles and red-tailed monkeys-Cercopithecus ascanius). Across all species (n = 71 samples), results demonstrated positive associations of organochlorine pesticides (OCPs) (ß = 0.143, p = 0.020) and organophosphate esters (ß = 0.112, p = 0.003) with cortisol in adult females. Additionally, we observed positive associations of OCPs (ß = 0.192, p = 0.013) and brominated flame retardants (ß = 0.176, p = 0.004) with cortisol in juveniles. Results suggest that cumulative pesticides and flame retardants are disruptive to endocrine function in these populations, which could have implications for development, metabolism and reproduction. Our study further demonstrates that faeces can be an important, non-invasive matrix for examining pollutant-hormone associations in wild primates and other critical wildlife populations.

Computational signatures of inequity aversion in children across seven societies.

[Correction Notice: An Erratum for this article was reported online in Journal of Experimental Psychology: General on Aug 10 2023 (see record 2023-96713-001). In the original article, there were affiliation errors for the first and 14th authors. The affiliations for Dorsa Amir are Department of Psychology, University of California, Berkeley; and Department of Psychology, Boston College. The affiliation for Katherine McAuliffe is Department of Psychology, Boston College. All versions of this article have been corrected.] Inequity aversion is an important factor in fairness behavior. Previous work suggests that children show more cross-cultural variation in their willingness to reject allocations that would give them more rewards than their partner-advantageous inequity-as opposed to allocations that would give them less than their partner-disadvantageous inequity. However, as past work has relied solely on children's decisions to accept or reject these offers, the algorithms underlying this pattern of variation remain unclear. Here, we explore the computational signatures of inequity aversion by applying a computational model of decision-making to data from children (N = 807) who played the Inequity Game across seven societies. Specifically, we used drift-diffusion models to formally distinguish evaluative processing (i.e., the computation of the subjective value of accepting or rejecting inequity) from alternative factors such as decision speed and response strategies. Our results suggest that variation in the development of inequity aversion across societies is best accounted for by variation in the drift rate-the direction and strength of the evaluative preference. Our findings underscore the utility of looking beyond decision data to better understand behavioral diversity. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Evolutionary and neuroendocrine foundations of human aggression.

Humans present a behavioural paradox: they are peaceful in many circumstances, but they are also violent and kill conspecifics at high rates. We describe a social evolutionary theory to resolve this paradox. The theory interprets human aggression as a combination of low propensities for reactive aggression and coercive behaviour and high propensities for some forms of proactive aggression (especially coalitionary proactive aggression). These tendencies are associated with the evolution of groupishness, self-domestication, and social norms. This human aggression profile is expected to demand substantial plasticity in the evolved biological mechanisms responsible for aggression. We discuss the contributions of various social signalling molecules (testosterone, cortisol, oxytocin, vasopressin, serotonin, and dopamine) as the neuroendocrine foundation conferring such plasticity.

Weak, but not strong, ties support coalition formation among wild female chimpanzees.

In social species, individuals may be able to overcome competitive constraints on cooperation by leveraging relationships with familiar, tolerant partners. While strong social ties have been linked to cooperation in several social mammals, it is unclear the extent to which weak social ties can support cooperation, particularly among non-kin. We tested the hypothesis that weakly affiliative social relationships support cooperative coalition formation using 10 years of behavioural data on wild female chimpanzees. Female chimpanzees typically disperse and reside with non-kin as adults. Their social relationships are differentiated but often relatively weak, with few dyads sharing strong bonds. Females occasionally form aggressive coalitions together. Three measures of relationship quality-party association, five-metre proximity and whether a dyad groomed-positively predicted coalitions, indicating that relationship quality influenced coalition partnerships. However, dyads that groomed frequently did not form more coalitions than dyads that groomed occasionally, and kin did not cooperate more than expected given their relationship quality. Thus, strong bonds and kinship did not bolster cooperation. We conclude that cooperative coalitions among female chimpanzees depend on social tolerance but do not require strong bonds. Our findings highlight social tolerance as a distinct pathway through which females can cultivate cooperative relationships. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Safeguarding human-wildlife cooperation.

Human-wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human-honeyguide and human-dolphin cooperation, but these are at risk of joining several inactive forms (including human-wolf and human-orca cooperation). Human-wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components-a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge-which face threats from ecological and cultural changes. To safeguard human-wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract.

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs.

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

Female reproduction and viral infection in a long-lived mammal.

For energetically limited organisms, life-history theory predicts trade-offs between reproductive effort and somatic maintenance. This is especially true of female mammals, for whom reproduction presents multifarious energetic and physiological demands. Here, we examine longitudinal changes in the gut virome (viral community) with respect to reproductive status in wild mature female chimpanzees Pan troglodytes schweinfurthii from two communities, Kanyawara and Ngogo, in Kibale National Park, Uganda. We used metagenomic methods to characterize viromes of individual chimpanzees while they were cycling, pregnant and lactating. Females from Kanyawara, whose territory abuts the park's boundary, had higher viral richness and loads (relative quantity of viral sequences) than females from Ngogo, whose territory is more energetically rich and located farther from large human settlements. Viral richness (total number of distinct viruses per sample) was higher when females were lactating than when cycling or pregnant. In pregnant females, viral richness increased with estimated day of gestation. Richness did not vary with age, in contrast to prior research showing increased viral abundance in older males from these same communities. Our results provide evidence of short-term physiological trade-offs between reproduction and infection, which are often hypothesized to constrain health in long-lived species.

Females undergo selection too.

Extending Campbell's (1999) staying alive theory (SAT) beyond aggression, we reviewed evidence that females are more self-protective than males. Many commentators provided additional supporting data. Sex differences in life-history adaptations, in the optimal relation between survival and reproduction, and in the mechanisms underlying trade-offs involved with self-protection remain important topics with numerous opportunities for improved understanding.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Viruses associated with ill health in wild chimpanzees.

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.

Self-protection as an adaptive female strategy.

Many male traits are well explained by sexual selection theory as adaptations to mating competition and mate choice, whereas no unifying theory explains traits expressed more in females. Anne Campbell's "staying alive" theory proposed that human females produce stronger self-protective reactions than males to aggressive threats because self-protection tends to have higher fitness value for females than males. We examined whether Campbell's theory has more general applicability by considering whether human females respond with greater self-protectiveness than males to other threats beyond aggression. We searched the literature for physiological, behavioral, and emotional responses to major physical and social threats, and found consistent support for females' responding with greater self-protectiveness than males. Females mount stronger immune responses to many pathogens; experience a lower threshold to detect, and lesser tolerance of, pain; awaken more frequently at night; express greater concern about physically dangerous stimuli; exert more effort to avoid social conflicts; exhibit a personality style more focused on life's dangers; react to threats with greater fear, disgust, and sadness; and develop more threat-based clinical conditions than males. Our findings suggest that in relation to threat, human females have relatively heightened protective reactions compared to males. The pervasiveness of this result across multiple domains suggests that general mechanisms might exist underlying females' unique adaptations. An understanding of such processes would enhance knowledge of female health and well-being.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Nutritional geometry of female chimpanzees (Pan troglodytes).

Primate foraging is influenced by the spatial and temporal distribution of foods, which may facilitate or constrain optimal nutrient intakes. Chimpanzees are frugivorous primates that mainly subsist on ripe fruit that is typically low in available protein (AP) and high in easily digestible carbohydrates. Because chimpanzees prefer ripe fruit and often eat it in large quantities compared with other foods, we hypothesized that protein intake would be tightly regulated while non-protein energy (NPE) would vary with fruit intake. To test this hypothesis, we conducted all-day follows on female chimpanzees, recorded all types of food consumed (i.e., drupes, figs, and non-fruit foods), estimated the nutritional contributions of these foods to daily NPE and AP intake and investigated how the ratio of NPE to AP varied due to changes in the types of foods consumed. Although the proportions of drupes, figs, and non-fruit foods varied in their diets, female chimpanzees maintained a relatively stable intake of AP while intake of NPE varied depending on the daily diet, demonstrating that like other frugivorous primates studied to date, chimpanzees prioritize protein. The mean daily ratio of NPE to AP was 7:1, which is similar to that of other frugivorous primates studied. Our results support the hypothesis that frugivorous animals may generally prioritize AP, while maximizing NPE intake within that constraint, and could shed light on aspects of human dietary evolution.