CD4 receptor diversity in chimpanzees protects against SIV infection.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4+ T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.

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.

Dexterity and technique in termite fishing by chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle, Republic of Congo.

Although the phenomenon of termite fishing by chimpanzees (Pan troglodytes) has historical and theoretical importance for primatology, we still have a limited understanding of how chimpanzees accomplish this activity, and in particular, about details of skilled actions and the nature of individual variation in fishing techniques. We examined movements, hand positions, grips, and other details from remote video footage of seven adult and subadult female chimpanzees using plant probes to extract Macrotermes muelleri termites from epigeal nests. Six chimpanzees used exclusively one hand (left or right) to grip the probe during termite fishing. All chimpanzees used the same repertoire of actions to insert, adjust, and withdraw the probe but differed in the frequency of use of particular actions. Chimpanzees have been described as eating termites in two ways-directly from the probe or by sweeping them from the probe with one hand. We describe a third technique: sliding the probe between the digits of one stationary hand as the probe is extracted from the nest. The sliding technique requires complementary bimanual coordination (extracting with one hand and grasping lightly with the other, at the same time). We highlight the importance of actions with two hands-one gripping, one assisting-in termite fishing and discuss how probing techniques are correlated with performance. Additional research on digital function and on environmental, organismic, and task constraints will further reveal manual dexterity in termite fishing.

Origin of the human malaria parasite Plasmodium falciparum in gorillas.

Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.

Lateralization and performance asymmetries in the termite fishing of wild chimpanzees in the goualougo triangle, republic of Congo.

The nearly universal right hand preference manifested by human populations is one of the most pronounced manifestations of population-level lateralization. Morphological and archeological evidence indicate that this behavioral specialization may have emerged among our hominin ancestors. Whether population-level behavioral asymmetries are evident in non-human animals remains a topic of considerable scientific debate, with the most consistent evidence of population-level trends emerging from studies of chimpanzees (Pan troglodytes). However, previous studies of population-level lateralization in wild apes have relied upon data sets pooled across populations to reach adequate sample sizes. Our aim was to test for population-level handedness within a single wild chimpanzee population, and also to determine if performance asymmetries were associated with handedness. To address these questions, we coded handedness and duration of fishing probe insertions from remote video footage of chimpanzee visitation to termite nests (totaling 119 hr) in the Goualougo Triangle, Republic of Congo. Similar to reports from other populations, chimpanzees in the Goualougo Triangle showed robust individual hand preferences for termite fishing. There were 46 right-handed, 39 left-handed, and 4 ambiguously-handed individuals. Though we did not detect an overall significant population-level handedness (t(88) = 0.83, n.s.) in this study, males showed a greater right hand preference than females. Further, we found that average dipping latencies were significantly faster for right- compared to left-handed chimpanzees. Possible explanations and evolutionary implications of taxa- and task-specific patterns of population-level laterality are discussed. Am. J. Primatol. 78:1190-1200, 2016. © 2016 Wiley Periodicals, Inc.

The interdigital brace and other grips for termite nest perforation by chimpanzees of the Goualougo Triangle, Republic of Congo.

Studies of chimpanzee termite foraging enlighten our understanding of early hominin tool use not only by modeling the cognitive ability of our ancestors but also by emphasizing the possible role of social insects in the hominin diet. The chimpanzees of the Goualougo Triangle are known to have one of the largest and most complex tool repertoires reported for wild chimpanzees. One tool set habitually used by this population includes a perforating tool to penetrate the hard outer crust of elevated termite nests before fishing for termite prey with an herbaceous stem. Here, we report the variation present in the grips used on the perforating tool. Our analysis of video recordings of chimpanzee visitation to termite nests over a 3-year period shows that these chimpanzees use a variety of grips to navigate the challenges encountered in opening a termite nest. For situations in which the soil is most hardened, perforating requires force and a power grip is often used. When the soil in the passageway is loose, precision grips are suitable for the task. One of the preferred grips reported here is an interdigital brace, which has previously been described in studies of how some people hold a pencil. In this study, for the first time, the interdigital brace has been thoroughly described for chimpanzees. The various strategies and grips used during perforation emphasize the importance of termites as a nutritional resource that should be considered more strongly as a food used by early hominins.

Insect prey characteristics affecting regional variation in chimpanzee tool use.

It is an ongoing interdisciplinary pursuit to identify the factors shaping the emergence and maintenance of tool technology. Field studies of several primate taxa have shown that tool using behaviors vary within and between populations. While similarity in tools over spatial and temporal scales may be the product of socially learned skills, it may also reflect adoption of convergent strategies that are tailored to specific prey features. Much has been claimed about regional variation in chimpanzee tool use, with little attention to the ecological circumstances that may have shaped such differences. This study examines chimpanzee tool use in termite gathering to evaluate the extent to which the behavior of insect prey may dictate chimpanzee technology. More specifically, we conducted a systematic comparison of chimpanzee tool use and termite prey between the Goualougo Triangle in the Republic of Congo and the La Belgique research site in southeast Cameroon. Apes at both of these sites are known to use tool sets to gather several species of termites. We collected insect specimens and measured the characteristics of their nests. Associated chimpanzee tool assemblages were documented at both sites and video recordings were conducted in the Goualougo Triangle. Although Macrotermitinae assemblages were identical, we found differences in the tools used to gather these termites. Based on measurements of the chimpanzee tools and termite nests at each site, we concluded that some characteristics of chimpanzee tools were directly related to termite nest structure. While there is a certain degree of uniformity within approaches to particular tool tasks across the species range, some aspects of regional variation in hominoid technology are likely adaptations to subtle environmental differences between populations or groups. Such microecological differences between sites do not negate the possibility of cultural transmission, as social learning may be required to transmit specific behaviors among individuals.

Portrayals of wild primates in documentary films: reason for concern?

Documentaries are the primary means by which many people observe the behavior of wild primates. By influencing layperson perceptions of wild primates, documentaries could impact viewer conservation-related beliefs and behaviors and, therefore, the well-being of wild primates. To investigate such portrayals, we examined documentaries depicting the four species that were most represented in documentaries: rhesus macaque, chimpanzee, ring-tailed lemur, and mountain gorilla. For each documentary, we continuously coded behavior, conducted scan samples of age-sex classes at 3-min intervals, and made ad libitum observations of inaccuracies and misleading content. We expected that representation of age-sex classes and activity budgets in documentaries would differ from those reported in the primary literature for the same species in the wild. In addition, we expected inaccurate depictions for every species. For ring-tailed lemurs, adult males were underrepresented in documentaries. For macaques, chimpanzees, and gorillas, representation of age-sex classes did not differ significantly from observations in the wild. Documentary depictions of activity budgets differed from researcher accounts of wild primate behavior for rhesus macaques, chimpanzees, and mountain gorillas, but not for ring-tailed lemurs. In general, documentaries overrepresented traveling and social behaviors such as play and grooming. Documentaries, especially docudramas, may have emphasized traveling because such footage allows storyline narration, whereas the emphasis on social behavior was likely due to the appeal of such footage to audiences. Inaccuracies were documented for all four species, with rhesus macaques having the most inaccuracies. We propose that primatologists have an ethical imperative to enhance the accuracy of primate portrayals to audiences.

Widespread extinctions of co-diversified primate gut bacterial symbionts from humans.

Humans and other primates harbour complex gut bacterial communities that influence health and disease, but the evolutionary histories of these symbioses remain unclear. This is partly due to limited information about the microbiota of ancestral primates. Here, using phylogenetic analyses of metagenome-assembled genomes (MAGs), we show that hundreds of gut bacterial clades diversified in parallel (that is, co-diversified) with primate species over millions of years, but that humans have experienced widespread losses of these ancestral symbionts. Analyses of 9,460 human and non-human primate MAGs, including newly generated MAGs from chimpanzees and bonobos, revealed significant co-diversification within ten gut bacterial phyla, including Firmicutes, Actinobacteriota and Bacteroidota. Strikingly, ~44% of the co-diversifying clades detected in African apes were absent from available metagenomic data from humans and ~54% were absent from industrialized human populations. In contrast, only ~3% of non-co-diversifying clades detected in African apes were absent from humans. Co-diversifying clades present in both humans and chimpanzees displayed consistent genomic signatures of natural selection between the two host species but differed in functional content from co-diversifying clades lost from humans, consistent with selection against certain functions. This study discovers host-species-specific bacterial symbionts that predate hominid diversification, many of which have undergone accelerated extinctions from human populations.

Malaria-driven adaptation of MHC class I in wild bonobo populations.

The malaria parasite Plasmodium falciparum causes substantial human mortality, primarily in equatorial Africa. Enriched in affected African populations, the B*53 variant of HLA-B, a cell surface protein that presents peptide antigens to cytotoxic lymphocytes, confers protection against severe malaria. Gorilla, chimpanzee, and bonobo are humans' closest living relatives. These African apes have HLA-B orthologs and are infected by parasites in the same subgenus (Laverania) as P. falciparum, but the consequences of these infections are unclear. Laverania parasites infect bonobos (Pan paniscus) at only one (TL2) of many sites sampled across their range. TL2 spans the Lomami River and has genetically divergent subpopulations of bonobos on each side. Papa-B, the bonobo ortholog of HLA-B, includes variants having a B*53-like (B07) peptide-binding supertype profile. Here we show that B07 Papa-B occur at high frequency in TL2 bonobos and that malaria appears to have independently selected for different B07 alleles in the two subpopulations.

The role of terrestriality in promoting primate technology.

"Complex technology" has often been considered a hallmark of human evolution. However, recent findings show that wild monkeys are also capable of habitual tool use. Here we suggest that terrestriality may have been of crucial importance for the innovation, acquisition, and maintenance of "complex" technological skills in primates. Here we define complex technological skills as tool-use variants that include at least two tool elements (for example, hammer and anvil), flexibility in manufacture or use (that is, tool properties are adjusted to the task at hand), and that skills are acquired in part by social learning. Four lines of evidence provide support for the terrestriality effect. First, the only monkey populations exhibiting habitual tool use seem to be particularly terrestrial. Second, semi-terrestrial chimpanzees have more complex tool variants in their repertoire than does their arboreal Asian relative, the orangutan. Third, tool variants of chimpanzees used in a terrestrial setting tend to be more complex than those used exclusively in arboreal contexts. Fourth, the higher frequency in tool use among captive versus wild primates of the same species may be attributed in part to a terrestriality effect. We conclude that whereas extractive foraging, intelligence, and social tolerance are necessary for the emergence of habitual tool use, terrestriality seems to be crucial for acquiring and maintaining complex tool variants, particularly expressions of cumulative technology, within a population. Hence, comparative evidence among primates supports the hypothesis that the terrestriality premium may have been a major pacemaker of hominin technological evolution.

A low-cost genomics workflow enables isolate screening and strain-level analyses within microbiomes.

Earth's environments harbor complex consortia of microbes that affect processes ranging from host health to biogeochemical cycles. Understanding their evolution and function is limited by an inability to isolate genomes in a high-throughput manner. Here, we present a workflow for bacterial whole-genome sequencing using open-source labware and the OpenTrons robotics platform, reducing costs to approximately $10 per genome. We assess genomic diversity within 45 gut bacterial species from wild-living chimpanzees and bonobos. We quantify intraspecific genomic diversity and reveal divergence of homologous plasmids between hosts. This enables population genetic analyses of bacterial strains not currently possible with metagenomic data alone.

Interspecific interactions between sympatric apes.

Gorillas reside in sympatry with chimpanzees over the majority of their range. Compiling all known reports of overlap between apes and augmenting these with observations made over twenty years in the Ndoki Forest, we examine the potential predation-related, foraging, and social contexts of interspecific associations between gorillas and chimpanzees. We reveal a greater diversity of interactions than previously recognized, which range from play to lethal aggression. Furthermore, there are indications that interactions between ape species may serve multiple functions. Interactions between gorillas and chimpanzees were most common during foraging activities, but they also overlapped in several other contexts. From a social perspective, we provide evidence of consistent relationships between particular chimpanzee-gorilla dyads. In addition to providing new insights into extant primate community dynamics, the diversity of interactions between apes points to an entirely new field of study in early human origins as early hominins also likely had opportunities to associate.

Zoonotic origin of the human malaria parasite Plasmodium malariae from African apes.

The human parasite Plasmodium malariae has relatives infecting African apes (Plasmodium rodhaini) and New World monkeys (Plasmodium brasilianum), but its origins remain unknown. Using a novel approach to characterise P. malariae-related sequences in wild and captive African apes, we found that this group comprises three distinct lineages, one of which represents a previously unknown, highly divergent species infecting chimpanzees, bonobos and gorillas across central Africa. A second ape-derived lineage is much more closely related to the third, human-infective lineage P. malariae, but exhibits little evidence of genetic exchange with it, and so likely represents a separate species. Moreover, the levels and nature of genetic polymorphisms in P. malariae indicate that it resulted from the zoonotic transmission of an African ape parasite, reminiscent of the origin of P. falciparum. In contrast, P. brasilianum falls within the radiation of human P. malariae, and thus reflects a recent anthroponosis.

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.

Molecular epidemiology of simian immunodeficiency virus infection in wild-living gorillas.

Chimpanzees and gorillas are the only nonhuman primates known to harbor viruses closely related to HIV-1. Phylogenetic analyses showed that gorillas acquired the simian immunodeficiency virus SIVgor from chimpanzees, and viruses from the SIVcpz/SIVgor lineage have been transmitted to humans on at least four occasions, leading to HIV-1 groups M, N, O, and P. To determine the geographic distribution, prevalence, and species association of SIVgor, we conducted a comprehensive molecular epidemiological survey of wild gorillas in Central Africa. Gorilla fecal samples were collected in the range of western lowland gorillas (n = 2,367) and eastern Grauer gorillas (n = 183) and tested for SIVgor antibodies and nucleic acids. SIVgor antibody-positive samples were identified at 2 sites in Cameroon, with no evidence of infection at 19 other sites, including 3 in the range of the Eastern gorillas. In Cameroon, based on DNA and microsatellite analyses of a subset of samples, we estimated the prevalence of SIVgor to be 1.6% (range, 0% to 4.6%), which is significantly lower than the prevalence of SIVcpzPtt in chimpanzees (5.9%; range, 0% to 32%). All newly identified SIVgor strains formed a monophyletic lineage within the SIVcpz radiation, closely related to HIV-1 groups O and P, and clustered according to their field site of origin. At one site, there was evidence for intergroup transmission and a high intragroup prevalence. These isolated hot spots of SIVgor-infected gorilla communities could serve as a source for human infection. The overall low prevalence and sporadic distribution of SIVgor could suggest a decline of SIVgor in wild populations, but it cannot be excluded that SIVgor is still more prevalent in other parts of the geographical range of gorillas.

Elemental variation in the termite fishing of wild chimpanzees (Pan troglodytes).

Chimpanzee tool behaviours vary dramatically in their complexity and extent of geographical distribution. The use of tool sets with specific design features to gather termites extends across a large portion of central Africa. Detailed examination of the composition and uniformity of such complex tool tasks has the potential to advance our understanding of the cognitive capabilities of tool users and processes underlying the maintenance of technological skills. In this study, we examined variation in chimpanzee tool use in termite gathering from video-recorded sequences that were scored to the level of functionally distinct behavioural elements. Overall, we found a high degree of similarity in tool-using techniques exhibited by individuals in this population. The number of elements in each individual's repertoire often exceeded that necessary to accomplish the task, with consistent differences in repertoire sizes between age classes. Adults and subadults had the largest repertoires and more consistently exhibited element strings than younger individuals. Larger repertoires were typically associated with incorporation of rare variants, some of which indicate flexibility and intelligence. These tool using apes aid us in understanding the evolution of technology, including that of our human ancestors, which showed a high degree of uniformity over large spatial scales.

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.

Chimpanzees prey on army ants with specialized tool set.

Several populations of chimpanzees have been reported to prey upon Dorylus army ants. The most common tool-using technique to gather these ants is with "dipping" probes, which vary in length with regard to aggressiveness and lifestyle of the prey species. We report the use of a tool set in army ant predation by chimpanzees in the Goualougo Triangle, Republic of Congo. We recovered 1,060 tools used in this context and collected 25 video recordings of chimpanzee tool-using behavior at ant nests. Two different types of tools were distinguished based on their form and function. The chimpanzees use a woody sapling to perforate the ant nest, and then a herb stem as a dipping tool to harvest the ants. All of the species of ants preyed upon in Goualougo are present and consumed by chimpanzees at other sites, but there are no other reports of such a regular or widespread use of more than one type of tool to prey upon Dorylus ants. Furthermore, this tool set differs from other types of tool combinations used by chimpanzees at this site for preying upon termites or gathering honey. Therefore, we conclude that these chimpanzees have developed a specialized method for preying upon army ants, which involves the use of an additional tool for opening nests. Further research is needed to determine which specific ecological and social factors may have shaped the emergence and maintenance of this technology.

Consistent differences in a virtual world model of ape societies.

Practical and ethical constraints limit our ability to experimentally test socioecological theory in wild primates. We took an alternate approach to model this, allowing groups of humans to interact in a virtual world in which they had to find food and interact with both ingroup and outgroup avatars to earn rewards. We altered ratios and distributions of high- and low-value foods to test the hypothesis that hominoids vary with regards to social cohesion and intergroup tolerance due to their feeding ecology. We found larger nesting clusters and decreased attacks on outgroup competitors in the Bonobo condition versus the Chimpanzee condition, suggesting a significant effect of feeding competition alone on social structure. We also demonstrate that virtual worlds are a robust mechanism for testing hypotheses that are impossible to study in the wild.