Potentially Zoonotic Enteric Infections in Gorillas and Chimpanzees, Cameroon and Tanzania.

Despite zoonotic potential, data are lacking on enteric infection diversity in wild apes. We employed a novel molecular diagnostic platform to detect enteric infections in wild chimpanzees and gorillas. Prevalent Cryptosporidium parvum, adenovirus, and diarrheagenic Escherichia coli across divergent sites and species demonstrates potential widespread circulation among apes in Africa.

Camera traps unveil demography, social structure, and home range of six unhabituated Western chimpanzee groups in the Moyen Bafing National Park, Guinea.

Precise estimates of population dynamics and social grouping patterns are required for effective conservation of wild animal populations. It is difficult to obtain such information on non-human great apes as they have slow reproductive rates. To gain a better understanding of demography in these populations, previous research has typically involved habituation\, a process that requires years. Here, we collected data continuously over year-long periods to monitor an unhabituated population of critically endangered Western chimpanzees (Pan troglodytes verus) in the Moyen Bafing National Park, Guinea. We used two arrays of 100 camera traps that were placed opportunistically in two distinct 100 km2 sites, named Bakoun and Koukoutamba. We identified 227 individuals in Bakoun and 207 in Koukoutamba through their unique facial features. Our camera trap data make clear that these individuals belong to six and seven closed groups, respectively. Six of those groups were near-completely sampled with an average minimum size of 46.8 individuals (range: 37-58), and a mean adult sex ratio of 1.32 (range: 0.93-2.10). We described the demographic composition of these groups and use Bayesian social network analysis to understand population structure. The network analyses suggested that the social bonds within the two populations were structured by sex homophily, with male chimpanzees being more or equally likely to be observed together than other adult associations. Through estimation of minimum convex polygons, we described the minimum home range for those groups. Compared to other chimpanzee groups living in a similar environment (mosaic savanna-forest), the Moyen Bafing region seems to host a high-density of chimpanzees with small home ranges for their group size. Our research highlights the potential of camera traps for studying the demographic composition of chimpanzee populations with high resolution and obtaining crucial information on several groups in a time-efficient and cost-effective way.

Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest.

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

Discovery of Novel Herpes Simplexviruses in Wild Gorillas, Bonobos, and Chimpanzees Supports Zoonotic Origin of HSV-2.

Viruses closely related to human pathogens can reveal the origins of human infectious diseases. Human herpes simplexvirus type 1 (HSV-1) and type 2 (HSV-2) are hypothesized to have arisen via host-virus codivergence and cross-species transmission. We report the discovery of novel herpes simplexviruses during a large-scale screening of fecal samples from wild gorillas, bonobos, and chimpanzees. Phylogenetic analysis indicates that, contrary to expectation, simplexviruses from these African apes are all more closely related to HSV-2 than to HSV-1. Molecular clock-based hypothesis testing suggests the divergence between HSV-1 and the African great ape simplexviruses likely represents a codivergence event between humans and gorillas. The simplexviruses infecting African great apes subsequently experienced multiple cross-species transmission events over the past 3 My, the most recent of which occurred between humans and bonobos around 1 Ma. These findings revise our understanding of the origins of human herpes simplexviruses and suggest that HSV-2 is one of the earliest zoonotic pathogens.

The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

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.

Nocturnal activity in wild chimpanzees (Pan troglodytes): Evidence for flexible sleeping patterns and insights into human evolution.

OBJECTIVES: We investigated occurrences and patterns of terrestrial nocturnal activity in wild chimpanzees (Pan troglodytes) and modelled the influence of various ecological predictors on nocturnal activity. METHODS: Data were extracted from terrestrial camera-trap footage and ecological surveys from 22 chimpanzee study sites participating in the Pan African Programme: The Cultured Chimpanzee. We described videos demonstrating nocturnal activity, and we tested the effects of the percentage of forest, abundance of predators (lions, leopards and hyenas), abundance of large mammals (buffalos and elephants), average daily temperature, rainfall, human activity, and percent illumination on the probability of nocturnal activity. RESULTS: We found terrestrial nocturnal activity to occur at 18 of the 22 study sites, at an overall average proportion of 1.80% of total chimpanzee activity, and to occur during all hours of the night, but more frequently during twilight hours. We found a higher probability of nocturnal activity with lower levels of human activity, higher average daily temperature, and at sites with a larger percentage of forest. We found no effect of the abundance of predators and large mammals, rainfall, or moon illumination. DISCUSSION: Chimpanzee terrestrial nocturnal activity appears widespread yet infrequent, which suggests a consolidated sleeping pattern. Nocturnal activity may be driven by the stress of high daily temperatures and may be enabled at low levels of human activity. Human activity may exert a relatively greater influence on chimpanzee nocturnal behavior than predator presence. We suggest that chimpanzee nocturnal activity is flexible, enabling them to respond to changing environmental factors.

Non-invasive genetic censusing and monitoring of primate populations.

Knowing the density or abundance of primate populations is essential for their conservation management and contextualizing socio-demographic and behavioral observations. When direct counts of animals are not possible, genetic analysis of non-invasive samples collected from wildlife populations allows estimates of population size with higher accuracy and precision than is possible using indirect signs. Furthermore, in contrast to traditional indirect survey methods, prolonged or periodic genetic sampling across months or years enables inference of group membership, movement, dynamics, and some kin relationships. Data may also be used to estimate sex ratios, sex differences in dispersal distances, and detect gene flow among locations. Recent advances in capture-recapture models have further improved the precision of population estimates derived from non-invasive samples. Simulations using these methods have shown that the confidence interval of point estimates includes the true population size when assumptions of the models are met, and therefore this range of population size minima and maxima should be emphasized in population monitoring studies. Innovations such as the use of sniffer dogs or anti-poaching patrols for sample collection are important to ensure adequate sampling, and the expected development of efficient and cost-effective genotyping by sequencing methods for DNAs derived from non-invasive samples will automate and speed analyses.

Long-term group membership and dynamics in a wild western lowland gorilla population (Gorilla gorilla gorilla) inferred using non-invasive genetics.

The social organization of a group-living animal is defined by a balance between group dynamic events such as group formation, group dissolution, and dispersal events and group stability in membership and over time. Understanding these processes, which are relevant for questions ranging from disease transmission patterns to the evolution of polygyny, requires long-term monitoring of multiple social units over time. Because all great ape species are long-lived and elusive, the number of studies on these key aspects of social organization are limited, especially for western lowland gorillas (Gorilla gorilla gorilla). In this study, we used non-invasive genetic samples collected within an approximately 100 km2 area of Loango National Park, Gabon to reconstruct group compositions and changes in composition over more than a decade. We identified 98 gorillas and 11 mixed sex groups sampled during 2014-2017. Using published data from 85 individuals and 12 groups surveyed between 2005 and 2009 at the same locality, we tracked groups and individuals back in time. The identification of 11 silverbacks via parentage analyses and the genetic tracking of 39 individuals across studies allowed us to infer six group formations, five group dissolutions, and 40 dispersal events within 12 years. We also observed four groups persisting across the sampling periods with a maximum inferred existence of nearly 17 years and exhibiting variation in membership stability. Our results highlight the variation in composition and stability among groups of western lowland gorillas and illustrate the power of non-invasive genetic sampling for long-term monitoring.

Chimpanzees routinely fish for algae with tools during the dry season in Bakoun, Guinea.

Wild chimpanzees regularly use tools, made from sticks, leaves, or stone, to find flexible solutions to the ecological challenges of their environment. Nevertheless, some studies suggest strong limitations in the tool-using capabilities of chimpanzees. In this context, we present the discovery of a newly observed tool-use behavior in a population of chimpanzees (Pan troglodytes verus) living in the Bakoun Classified Forest, Guinea, where a temporary research site was established for 15 months. Bakoun chimpanzees of every age-sex class were observed to fish for freshwater green algae, Spirogrya sp., from rivers, streams, and ponds using long sticks and twigs, ranging from 9 cm up to 4.31 m in length. Using remote camera trap footage from 11 different algae fishing sites within an 85-km2 study area, we found that algae fishing occurred frequently during the dry season and was non-existent during the rainy season. Chimpanzees were observed algae fishing for as little as 1 min to just over an hour, with an average duration of 9.09 min. We estimate that 364 g of Spirogyra algae could be retrieved in this time, based on human trials in the field. Only one other chimpanzee population living in Bossou, Guinea, has been described to customarily scoop algae from the surface of the water using primarily herbaceous tools. Here, we describe the new behavior found at Bakoun and compare it to the algae scooping observed in Bossou chimpanzees and the occasional variant reported in Odzala, Republic of the Congo. As these algae are reported to be high in protein, carbohydrates, and minerals, we hypothesize that chimpanzees are obtaining a nutritional benefit from this seasonally available resource.

The Maf factor Traffic jam both enables and inhibits collective cell migration in Drosophila oogenesis.

Border cell cluster (BCC) migration in the Drosophila ovary is an excellent system to study the gene regulatory network that enables collective cell migration. Here, we identify the large Maf transcription factor Traffic jam (Tj) as an important regulator of BCC migration. Tj has a multifaceted impact on the known core cascade that enables BCC motility, consisting of the Jak/Stat signaling pathway, the C/EBP factor Slow border cells (Slbo), and the downstream effector DE-cadherin (DEcad). The initiation of BCC migration coincides with a Slbo-dependent decrease in Tj expression. This reduction of Tj is required for normal BCC motility, as high Tj expression strongly impedes migration. At high concentration, Tj has a tripartite negative effect on the core pathway: a decrease in Slbo, an increase in the Jak/Stat inhibitor Socs36E, and a Slbo-independent reduction of DEcad. However, maintenance of a low expression level of Tj in the BCC during migration is equally important, as loss of tj function also results in a significant delay in migration concomitant with a reduction of Slbo and consequently of DEcad. Taken together, we conclude that the regulatory feedback loop between Tj and Slbo is necessary for achieving the correct activity levels of migration-regulating factors to ensure proper BCC motility.

The sampling scheme matters: Pan troglodytes troglodytes and P. t. schweinfurthii are characterized by clinal genetic variation rather than a strong subspecies break.

Populations of an organism living in marked geographical or evolutionary isolation from other populations of the same species are often termed subspecies and expected to show some degree of genetic distinctiveness. The common chimpanzee (Pan troglodytes) is currently described as four geographically delimited subspecies: the western (P. t. verus), the nigerian-cameroonian (P. t. ellioti), the central (P. t. troglodytes) and the eastern (P. t. schweinfurthii) chimpanzees. Although these taxa would be expected to be reciprocally monophyletic, studies have not always consistently resolved the central and eastern chimpanzee taxa. Most studies, however, used data from individuals of unknown or approximate geographic provenance. Thus, genetic data from samples of known origin may shed light on the evolutionary relationship of these subspecies. We generated microsatellite genotypes from noninvasively collected fecal samples of 185 central chimpanzees that were sampled across large parts of their range and analyzed them together with 283 published eastern chimpanzee genotypes from known localities. We observed a clear signal of isolation by distance across both subspecies. Further, we found that a large proportion of comparisons between groups taken from the same subspecies showed higher genetic differentiation than the least differentiated between-subspecies comparison. This proportion decreased substantially when we simulated a more clumped sampling scheme by including fewer groups. Our results support the general concept that the distribution of the sampled individuals can dramatically affect the inference of genetic population structure. With regard to chimpanzees, our results emphasize the close relationship of equatorial chimpanzees from central and eastern equatorial Africa and the difficult nature of subspecies definitions.

Genetic censusing identifies an unexpectedly sizeable population of an endangered large mammal in a fragmented forest landscape.

BACKGROUND: As habitat degradation and fragmentation continue to impact wildlife populations around the world, it is critical to understand the behavioral flexibility of species in these environments. In Uganda, the mostly unprotected forest fragment landscape between the Budongo and Bugoma Forests is a potential corridor for chimpanzees, yet little is known about the status of chimpanzee populations in these fragments. RESULTS: From 2011 through 2013, we noninvasively collected 865 chimpanzee fecal samples across 633 km(2) and successfully genotyped 662 (77%) at up to 14 microsatellite loci. These genotypes corresponded to 182 chimpanzees, with a mean of 3.5 captures per individual. We obtained population size estimates of 256 (95% confidence interval 246-321) and 319 (288-357) chimpanzees using capture-with-replacement and spatially explicit capture-recapture models, respectively. The spatial clustering of associated genotypes suggests the presence of at least nine communities containing a minimum of 8-33 individuals each. Putative community distributions defined by the locations of associated genotypes correspond well with the distribution of 14 Y-chromosome haplotypes. CONCLUSIONS: These census figures are more than three times greater than a previous estimate based on an extrapolation from small-scale nest count surveys that tend to underestimate population size. The distribution of genotype clusters and Y-chromosome haplotypes together indicate the presence of numerous male philopatric chimpanzee communities throughout the corridor habitat. Our findings demonstrate that, despite extensive habitat loss and fragmentation, chimpanzees remain widely distributed and exhibit distinct community home ranges. Our results further imply that elusive and rare species may adapt to degraded habitats more successfully than previously believed. Their long-term persistence is unlikely, however, if protection is not afforded to them and habitat loss continues unabated.

Characterization of MHC class II B polymorphism in multiple populations of wild gorillas using non-invasive samples and next-generation sequencing.

Genes encoded by the major histocompatibility complex (MHC) are crucial for the recognition and presentation of antigens to the immune system. In contrast to their closest relatives, chimpanzees and humans, much less is known about variation in gorillas at these loci. This study explored the exon 2 variation of -DPB1, -DQB1, and -DRB genes in 46 gorillas from four populations while simultaneously evaluating the feasibility of using fecal samples for high-throughput MHC genotyping. By applying strict similarity- and frequency-based analysis, we found, despite our modest sample size, a total of 18 alleles that have not been described previously, thereby illustrating the potential for efficient and highly accurate MHC genotyping from non-invasive DNA samples. We emphasize the importance of controlling for multiple potential sources of error when applying this massively parallel short-read sequencing technology to PCR products generated from low concentration DNA extracts. We observed pronounced differences in MHC variation between species, subspecies and populations that are consistent with both the ancient and recent demographic histories experienced by gorillas.

Recent divergences and size decreases of eastern gorilla populations.

Compared with other African apes, eastern gorillas (Gorilla beringei) have been little studied genetically. We used analysis of autosomal DNA genotypes obtained from non-invasively collected faecal samples to estimate the evolutionary histories of the two extant mountain gorilla populations and the closely related eastern lowland gorillas. Our results suggest that eastern lowland gorillas and mountain gorillas split beginning some 10 000 years ago, followed 5000 years ago by the split of the two mountain gorilla populations of Bwindi Impenetrable National Park and the Virungas Massif. All three populations have decreased in effective population size, with particularly substantial 10-fold decreases for the mountain gorillas. These dynamics probably reflect responses to habitat changes resulting from climate fluctuations over the past 20 000 years as well as increasing human influence in this densely populated region in the last several thousand years.

The genetic population structure of wild western lowland gorillas (Gorilla gorilla gorilla) living in continuous rain forest.

To understand the evolutionary histories and conservation potential of wild animal species it is useful to assess whether taxa are genetically structured into different populations and identify the underlying factors responsible for any clustering. Landscape features such as rivers may influence genetic population structure, and analysis of structure by sex can further reveal effects of sex-specific dispersal. Using microsatellite genotypes obtained from noninvasively collected fecal samples we investigated the population structure of 261 western lowland gorillas (WLGs) (Gorilla gorilla gorilla) from seven locations spanning an approximately 37,000 km(2) region of mainly continuous rain forest within Central African Republic (CAR), Republic of Congo and Cameroon. We found our sample to consist of two or three significantly differentiated clusters. The boundaries of the clusters coincided with courses of major rivers. Moreover, geographic distance detoured around rivers better-explained variation in genetic distance than straight line distance. Together these results suggest that major rivers in our study area play an important role in directing WLG gene flow. The number of clusters did not change when males and females were analyzed separately, indicating a lack of greater philopatry in WLG females than males at this scale.

Threat of mining to African great apes.

The rapid growth of clean energy technologies is driving a rising demand for critical minerals. In 2022 at the 15th Conference of the Parties to the Convention on Biological Diversity (COP15), seven major economies formed an alliance to enhance the sustainability of mining these essential decarbonization minerals. However, there is a scarcity of studies assessing the threat of mining to global biodiversity. By integrating a global mining dataset with great ape density distribution, we estimated the number of African great apes that spatially coincided with industrial mining projects. We show that up to one-third of Africa's great ape population faces mining-related risks. In West Africa in particular, numerous mining areas overlap with fragmented ape habitats, often in high-density ape regions. For 97% of mining areas, no ape survey data are available, underscoring the importance of increased accessibility to environmental data within the mining sector to facilitate research into the complex interactions between mining, climate, biodiversity, and sustainability.

Historical sampling reveals dramatic demographic changes in western gorilla populations.

BACKGROUND: Today many large mammals live in small, fragmented populations, but it is often unclear whether this subdivision is the result of long-term or recent events. Demographic modeling using genetic data can estimate changes in long-term population sizes while temporal sampling provides a way to compare genetic variation present today with that sampled in the past. In order to better understand the dynamics associated with the divergences of great ape populations, these analytical approaches were applied to western gorillas (Gorilla gorilla) and in particular to the isolated and Critically Endangered Cross River gorilla subspecies (G. g. diehli). RESULTS: We used microsatellite genotypes from museum specimens and contemporary samples of Cross River gorillas to infer both the long-term and recent population history. We find that Cross River gorillas diverged from the ancestral western gorilla population ~17,800 years ago (95% HDI: 760, 63,245 years). However, gene flow ceased only ~420 years ago (95% HDI: 200, 16,256 years), followed by a bottleneck beginning ~320 years ago (95% HDI: 200, 2,825 years) that caused a 60-fold decrease in the effective population size of Cross River gorillas. Direct comparison of heterozygosity estimates from museum and contemporary samples suggests a loss of genetic variation over the last 100 years. CONCLUSIONS: The composite history of western gorillas could plausibly be explained by climatic oscillations inducing environmental changes in western equatorial Africa that would have allowed gorilla populations to expand over time but ultimately isolate the Cross River gorillas, which thereafter exhibited a dramatic population size reduction. The recent decrease in the Cross River population is accordingly most likely attributable to increasing anthropogenic pressure over the last several hundred years. Isolation of diverging populations with prolonged concomitant gene flow, but not secondary admixture, appears to be a typical characteristic of the population histories of African great apes, including gorillas, chimpanzees and bonobos.

Limited evidence of C4 plant consumption in mound building Macrotermes termites from savanna woodland chimpanzee sites.

Stable isotope analysis is an increasingly used molecular tool to reconstruct the diet and ecology of elusive primates such as unhabituated chimpanzees. The consumption of C4 plant feeding termites by chimpanzees may partly explain the relatively high carbon isotope values reported for some chimpanzee communities. However, the modest availability of termite isotope data as well as the diversity and cryptic ecology of termites potentially consumed by chimpanzees obscures our ability to assess the plausibility of these termites as a C4 resource. Here we report the carbon and nitrogen isotope values from 79 Macrotermes termite samples from six savanna woodland chimpanzee research sites across equatorial Africa. Using mixing models, we estimated the proportion of Macrotermes C4 plant consumption across savanna woodland sites. Additionally, we tested for isotopic differences between termite colonies in different vegetation types and between the social castes within the same colony in a subset of 47 samples from 12 mounds. We found that Macrotermes carbon isotope values were indistinguishable from those of C3 plants. Only 5 to 15% of Macrotermes diets were comprised of C4 plants across sites, suggesting that they cannot be considered a C4 food resource substantially influencing the isotope signatures of consumers. In the Macrotermes subsample, vegetation type and caste were significantly correlated with termite carbon values, but not with nitrogen isotope values. Large Macrotermes soldiers, preferentially consumed by chimpanzees, had comparably low carbon isotope values relative to other termite castes. We conclude that Macrotermes consumption is unlikely to result in high carbon isotope values in either extant chimpanzees or fossil hominins.

Chimpanzee identification and social network construction through an online citizen science platform.

Citizen science has grown rapidly in popularity in recent years due to its potential to educate and engage the public while providing a means to address a myriad of scientific questions. However, the rise in popularity of citizen science has also been accompanied by concerns about the quality of data emerging from citizen science research projects. We assessed data quality in the online citizen scientist platform Chimp&See, which hosts camera trap videos of chimpanzees (Pan troglodytes) and other species across Equatorial Africa. In particular, we compared detection and identification of individual chimpanzees by citizen scientists with that of experts with years of experience studying those chimpanzees. We found that citizen scientists typically detected the same number of individual chimpanzees as experts, but assigned far fewer identifications (IDs) to those individuals. Those IDs assigned, however, were nearly always in agreement with the IDs provided by experts. We applied the data sets of citizen scientists and experts by constructing social networks from each. We found that both social networks were relatively robust and shared a similar structure, as well as having positively correlated individual network positions. Our findings demonstrate that, although citizen scientists produced a smaller data set based on fewer confirmed IDs, the data strongly reflect expert classifications and can be used for meaningful assessments of group structure and dynamics. This approach expands opportunities for social research and conservation monitoring in great apes and many other individually identifiable species.