Social and economic interdependence as a basis for peaceful between-group relationships in nonhuman primates and humans.

Glowacki asserts that interdependent relationships beyond group boundaries are exceptionally rare among nonhuman mammals. However, rudimentary forms of interdependence can be seen in primate species that form multilevel societies, that is, core social units embedded within higher-level grouping categories. Studies of primate multilevel societies can enrich discussions about the evolutionary origins of peaceful between-group interactions in humans.

Adaptations to a cold climate promoted social evolution in Asian colobine primates.

The biological mechanisms that underpin primate social evolution remain poorly understood. Asian colobines display a range of social organizations, which makes them good models for investigating social evolution. By integrating ecological, geological, fossil, behavioral, and genomic analyses, we found that colobine primates that inhabit colder environments tend to live in larger, more complex groups. Specifically, glacial periods during the past 6 million years promoted the selection of genes involved in cold-related energy metabolism and neurohormonal regulation. More-efficient dopamine and oxytocin pathways developed in odd-nosed monkeys, which may have favored the prolongation of maternal care and lactation, increasing infant survival in cold environments. These adaptive changes appear to have strengthened interindividual affiliation, increased male-male tolerance, and facilitated the stepwise aggregation from independent one-male groups to large multilevel societies.

Preference for Male Risk Takers Varies with Relationship Context and Health Status but not COVID Risk.

Risk taking is more commonly shown by males than females and has a signalling function, serving to advertise one's intrinsic quality to prospective mates. Previous research has established that male risk takers are judged as more attractive for short-term flings than long-term relationships, but the environmental and socioeconomic context surrounding female preferences for male risk takers has been overlooked. Using a survey instrument, we examined female preferences for male risk takers across 1304 females from 47 countries. We found preferences for physical risk takers to be more pronounced in females with a bisexual orientation and females who scored high on risk proneness. Self-reported health was positively associated with preferences for high risk takers as short-term mates, but the effect was moderated by country-level health, i.e. the association was stronger in countries with poorer health. The security provided by better health and access to health care may allow females to capitalise on the genetic quality afforded by selecting a risk-prone male whilst concurrently buffering the potential costs associated with the risk taker's lower paternal investment. The risk of contracting COVID-19 did not predict avoidance of risk takers, perhaps because this environmental cue is too novel to have moulded our behavioural preferences. Supplementary Information: The online version contains supplementary material available at 10.1007/s40806-023-00354-3.

Correlated evolution of social organization and lifespan in mammals.

Discerning the relationship between sociality and longevity would permit a deeper understanding of how animal life history evolved. Here, we perform a phylogenetic comparative analysis of ~1000 mammalian species on three states of social organization (solitary, pair-living, and group-living) and longevity. We show that group-living species generally live longer than solitary species, and that the transition rate from a short-lived state to a long-lived state is higher in group-living than non-group-living species, altogether supporting the correlated evolution of social organization and longevity. The comparative brain transcriptomes of 94 mammalian species identify 31 genes, hormones and immunity-related pathways broadly involved in the association between social organization and longevity. Further selection features reveal twenty overlapping pathways under selection for both social organization and longevity. These results underscore a molecular basis for the influence of the social organization on longevity.

The 10th anniversary of the scientific description of the black snub-nosed monkey (Rhinopithecus strykeri): It is time to initiate a set of new management strategies to save this critically endangered primate from extinction.

Traditionally, the genus Rhinopithecus (Milne-Edwards, 1872, Primates, Colobinae) included four allopatric species, restricted in their distributions to China and Vietnam. In 2010, a fifth species, the black snub-nosed monkey (Rhinopithecus strykeri) was discovered in the Gaoligong Mountains located on the border between China and Myanmar. Despite the remoteness, complex mountainous terrain, dense fog, and armed conflict that characterizes this region, over this past decade Chinese and Myanmar scientists have begun to collect quantitative data on the ecology, behavior and conservation requirements of R. strykeri. In this article, we review the existing data and present new information on the life history, ecology, and population size of R. strykeri. We discuss these data in the context of past and current conservation challenges faced by R. strykeri, and propose a series of both short-term and long-term management actions to ensure the survival of this Critically Endangered primate species. Specifically, we recommend that the governments and stakeholders in China and Myanmar formulate a transboundary conservation agreement that includes a consensus on bilateral exchange mechanisms, scientific research and monitoring goals, local community development, cooperation to prevent the hunting of endangered species and cross-border forest fires. These actions will contribute to the long-term conservation and survival of this Critically Endangered species.

Dissecting the two mechanisms of scramble competition among the Virunga mountain gorillas.

ABSTRACT: Two mechanisms have been proposed to explain why scramble competition can increase the travel requirements of individuals within larger groups. Firstly, individuals in larger groups may be more likely to encounter food sites where other group members have already eaten, leading to greater asynchronous "individual" travel to find fresh sites. Secondly, when food sites are aggregated into patches, larger groups may need to visit more patches to obtain the same amount of food per capita, leading to greater synchronous "group" travel between patches. If the first mechanism can be mitigated by increasing group spread, then we expect the second mechanism to be more sensitive to group size. Here, we examine the individual travel and group travel of the Virunga mountain gorillas, along with potential implications for the two mechanisms of scramble competition. Asynchronous individual travel accounted for 67% of the total travel time, and the remainder arose from group travel. Group spread increased significantly for larger groups, but not enough to prevent an increase in individual travel. Contrary to expectations, group travel decreased with size among most groups, and we found only limited evidence of patch depletion that would cause the second mechanism of scramble competition. Collectively, our results illustrate how the influence of group size can differ for individual travel versus group travel, just as it differs among species for overall travel. Studies that distinguish between the two mechanisms of scramble competition may enhance our understanding of ecological constraints upon group size, including potential differences between frugivores and folivores. SIGNIFICANCE STATEMENT: Feeding competition provides insight into how group size can influence the foraging patterns of social animals, but two key mechanisms are not typically compared. Firstly, larger groups may visit more patches to access the same amount of food per capita (group travel). Secondly, their individuals may also need to move past more spots where another member has already eaten (individual travel). Contrary to expectations, we found that group travel decreased with size for most groups of mountain gorillas, which may reflect extra travel by smaller groups to avoid larger groups. Individual travel increased with size in most groups, even though gorillas in larger groups compensated by spreading out over a broader area. The two mechanisms revealed patterns that were not apparent in our previous study of overall travel. Our approach may help to explain potential differences between folivores and frugivores.

Determinants of Harem Size in a Polygynous Primate: Reproductive Success and Social Benefits.

We used long-term data on the variation in harem size in Yunnan snub-nosed monkeys to research the effects of harem size on reproductive success and the ratio of grooming received to given (RGRG). The results suggest that harem holders derive reproductive benefits commensurate with harem size, whereas the females' reproductive success is unaffected by harem size. Males of larger harems groomed less and had higher RGRG than males of smaller harems. In the case of females, grooming given increased, and RGRG decreased with an increase in harem size. The males' reproductive success seems to be a driver of harem size maximization. From the females' perspective, dwindling social benefits appear to set the upper limit for harem enlargement. We also showed that males of monogamous units ('single-female harems') invested more into grooming their female, presumably to prevent unit disintegration and loss of mating privileges.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Do we need to reclassify the social systems of gregarious apes?

Decades of research have led to a solid understanding of the social systems of gregarious apes: chimpanzees, bonobos, gorillas, and gibbons. As field studies have increasingly collected data from multiple neighboring habituated groups, genetic and social interconnections have been revealed. These findings provide a more nuanced picture of intergroup relations in apes, and have led to claims in the literature that some ape taxa have multilevel societies. A multilevel society is defined as a nested collection of social entities comprising at least two discernible levels of social integration between the individual and the population. We argue that the evidence for multilevel sociality sensu stricto in apes is currently inconclusive and that it is premature to abandon the traditional classification of ape social systems. However, available findings appear to be consistent with the existence of some degree of higher social grouping patterns. We propose the term supra-group organization which may adequately capture ape social systems when viewed from a top-down perspective.

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

Chimpanzees Use Least-Cost Routes to Out-of-Sight Goals.

While the ability of naturally ranging animals to recall the location of food resources and use straight-line routes between them has been demonstrated in several studies [1, 2], it is not known whether animals can use knowledge of their landscape to walk least-cost routes [3]. This ability is likely to be particularly important for animals living in highly variable energy landscapes, where movement costs are exacerbated [4, 5]. Here, we used least-cost modeling, which determines the most efficient route assuming full knowledge of the environment, to investigate whether chimpanzees (Pan troglodytes) living in a rugged, montane environment walk least-cost routes to out-of-sight goals. We compared the "costs" and geometry of observed movements with predicted least-cost routes and local knowledge (agent-based) and straight-line null models. The least-cost model performed better than the local knowledge and straight-line models across all parameters, and linear mixed modeling showed a strong relationship between the cost of observed chimpanzee travel and least-cost routes. Our study provides the first example of the ability to take least-cost routes to out-of-sight goals by chimpanzees and suggests they have spatial memory of their home range landscape. This ability may be a key trait that has enabled chimpanzees to maintain their energy balance in a low-resource environment. Our findings provide a further example of how the advanced cognitive complexity of hominins may have facilitated their adaptation to a variety of environmental conditions and lead us to hypothesize that landscape complexity may play a role in shaping cognition.

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

Male social rank and food competition in a primate multi-level society.

OBJECTIVES: Social animals often have dominance hierarchies, with high rank conferring preferential access to resources. In primates, competition among males is often assumed to occur predominantly over reproductive opportunities. However, competition for food may occur during food shortages, such as in temperate species during winter. Higher-ranked males may thus gain preferential access to high-profitability food, which would enable them to spend longer engaged in activities other than feeding. MATERIALS AND METHODS: We performed a field experiment with a breeding band of golden snub-nosed monkeys, a species that lives in a multi-level society in high-altitude forests in central China. We provisioned monkey's high-profitability food during winter when natural foods are limited, and then recorded the times individual adult males spent engaged in different behaviors. RESULTS: Higher-ranking males spent less time feeding overall and fed on provisioned foods at a higher rate than lower-ranking males. Higher-ranking males therefore had more time to spend on alternative behaviors. We found no significant difference according to rank in times spent moving or resting. However, high-ranking males spend significantly longer on affiliative behaviors with other members of their social sub-units, especially grooming and being groomed, behaviors known to promote social cohesion in primates. DISCUSSION: We show that preferential access to high-profitability foods likely relaxes time-budget constraints to higher-ranking males. High-ranking males thus spend more time on non-feeding activities, especially grooming, which may enhance social cohesion within their social sub-unit. We discuss the potential direct and indirect benefits to high-ranking males associated with preferential access to high-value food during winter.

A comparison of fecal sampling and direct feeding observations for quantifying the diet of a frugivorous primate.

Both observational and indirect evidence are widely used to determine the diets of wild animals. Direct observations are often assumed to provide the most comprehensive reflection of diet, but many wild animals are logistically challenging to observe. Despite the regular use of observational and indirect methods for inferring diet in wild animals, they have rarely been compared in detail for the same study population. Over 12 months this study assessed the congruence of methods in estimating the diet of a montane community of eastern chimpanzees Pan troglodytes schweinfurthii in Nyungwe National Park, Rwanda using observational scan samples and macroscopic fecal inspection. The assessment of the number of food species consumed each month was comparable between methods, but the estimation of the composition of items in the diet differed significantly. Most notably, the fecal samples significantly underestimated the consumption of flowers, and certain fruit species, which based on direct behavioral observations were seasonally consumed at very high rates. Conversely, direct observations underestimated the consumption of leaves and pith in comparison to results present in the fecal samples. These results suggest that combining methods where possible is most useful for accurate monitoring of dietary trends, particularly for species that experience significant seasonal shifts in their diet.

Multilevel Organisation of Animal Sociality.

Multilevel societies (MLSs), stable nuclear social units within a larger collective encompassing multiple nested social levels, occur in several mammalian lineages. Their architectural complexity and size impose specific demands on their members requiring adaptive solutions in multiple domains. The functional significance of MLSs lies in their members being equipped to reap the benefits of multiple group sizes. Here, we propose a unifying terminology and operational definition of MLS. To identify new avenues for integrative research, we synthesise current literature on the selective pressures underlying the evolution of MLSs and their implications for cognition, intersexual conflict, and sexual selection. Mapping the drivers and consequences of MLS provides a reference point for the social evolution of many taxa, including our own species.