Local genetic adaptation to habitat in wild chimpanzees.

How populations adapt to their environment is a fundamental question in biology. Yet we know surprisingly little about this process, especially for endangered species such as non-human great apes. Chimpanzees, our closest living relatives, are particularly interesting because they inhabit diverse habitats, from rainforest to woodland-savannah. Whether genetic adaptation facilitates such habitat diversity remains unknown, despite having wide implications for evolutionary biology and conservation. Using 828 newly generated exomes from wild chimpanzees, we find evidence of fine-scale genetic adaptation to habitat. Notably, adaptation to malaria in forest chimpanzees is mediated by the same genes underlying adaptation to malaria in humans. This work demonstrates the power of non-invasive samples to reveal genetic adaptations in endangered populations and highlights the importance of adaptive genetic diversity for chimpanzees.

Population dynamics and genetic connectivity in recent chimpanzee history.

Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

Prevalence of antibodies against human respiratory viruses potentially involving anthropozoonoses in wild bonobos.

One of the current threats to the bonobo (Pan paniscus), a highly endangered ape species only found in the Democratic Republic of the Congo, are anthropozoonoses caused by human respiratory viruses. To date, epidemiological information regarding respiratory viral infections in bonobos is limited. In this study, we examined fecal immunoglobulin A antibodies against human respiratory viruses in bonobos, which may help estimating the viral prevalence. A substantial proportion of bonobos were positive for the antiviral antibodies, including those against parainfluenza virus, respiratory syncytial virus, influenza virus, rhinovirus, and mumps virus. The prevalence of the antibodies was found to depend on the viral species and bonobo populations, suggesting that the bonobos had been exposed to these respiratory viruses. These results may indicate the need for an epidemiological evidence-based action plan for the protection of bonobos from anthropozoonoses.

Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species.

Malaria parasites, though widespread among wild chimpanzees and gorillas, have not been detected in bonobos. Here, we show that wild-living bonobos are endemically Plasmodium infected in the eastern-most part of their range. Testing 1556 faecal samples from 11 field sites, we identify high prevalence Laverania infections in the Tshuapa-Lomami-Lualaba (TL2) area, but not at other locations across the Congo. TL2 bonobos harbour P. gaboni, formerly only found in chimpanzees, as well as a potential new species, Plasmodium lomamiensis sp. nov. Rare co-infections with non-Laverania parasites were also observed. Phylogenetic relationships among Laverania species are consistent with co-divergence with their gorilla, chimpanzee and bonobo hosts, suggesting a timescale for their evolution. The absence of Plasmodium from most field sites could not be explained by parasite seasonality, nor by bonobo population structure, diet or gut microbiota. Thus, the geographic restriction of bonobo Plasmodium reflects still unidentified factors that likely influence parasite transmission.

The mitochondrial ancestor of bonobos and the origin of their major haplogroups.

We report here where the most recent common ancestor (MRCA) of bonobos (Pan paniscus) ranged and how they dispersed throughout their current habitat. Mitochondrial DNA (mtDNA) molecular dating to analyze the time to MRCA (TMRCA) and the major mtDNA haplogroups of wild bonobos were performed using new estimations of divergence time of bonobos from other Pan species to investigate the dispersal routes of bonobos over the forest area of the Congo River's left bank. The TMRCA of bonobos was estimated to be 0.64 or 0.95 million years ago (Ma). Six major haplogroups had very old origins of 0.38 Ma or older. The reconstruction of the ancestral area revealed the mitochondrial ancestor of the bonobo populations ranged in the eastern area of the current bonobos' habitat. The haplogroups may have been formed from either the riparian forests along the Congo River or the center of the southern Congo Basin. Fragmentation of the forest refugia during the cooler periods may have greatly affected the formation of the genetic structure of bonobo populations.

Epidemiological Surveillance of Lymphocryptovirus Infection in Wild Bonobos.

Lymphocryptovirus (LCV) is one of the major gena in the herpesvirus family and is widely disseminated among primates. LCVs of human and rhesus macaques are shown to be causative agents of a number of malignant diseases including lymphoma and carcinoma. Bonobos (Pan paniscus) are highly endangered and the least studied species of the great apes. Considering the potential pathogenicity of the LCV that might threaten the fate of wild bonobos, population-based epidemiological information in terms of LCV prevalence in different location of Bonobo's habitats will help propose improved conservation strategies for the bonobos. However, such data are not available yet because it is very difficult to collect blood samples in the wild and thus virtually impossible to conduct sero-epidemiological study on the wild ape. In order to overcome this issue, we focused on evaluating anti-LCV IgA in the feces of bonobos, which are available in a non-invasive manner. Preliminary study showed that anti-LCV IgA but not IgG was efficiently and reproducibly detected in the feces of captive chimpanzees. It is noteworthy that the fecal IgA-positive individuals were seropositive for both anti-LCV IgG and IgA and that the IgA antibodies in both sera and feces were also detectable by Western blotting assay. These results indicate that the detection of fecal anti-LCV IgA is likely a reliable and feasible for epidemiological surveillance of LCV prevalence in the great apes. We then applied this method and found that 31% of wild bonobos tested were positive for anti-LCV IgA antibody in the feces. Notably, the positivity rates varied extensively among their sampled populations. In conclusion, our results in this study demonstrate that LCV is highly disseminated among wild bonobos while the prevalence is remarkably diverse in their population-dependent manner.

Correlates of bushmeat in markets and depletion of wildlife.

We used data on number of carcasses of wildlife species sold in 79 bushmeat markets in a region of Nigeria and Cameroon to assess whether species composition of a market could be explained by anthropogenic pressures and environmental variables around each market. More than 45 mammal species from 9 orders were traded across all markets; mostly ungulates and rodents. For each market, we determined median body mass, species diversity (game diversity), and taxa that were principal contributors to the total number of carcasses for sale (game dominance). Human population density in surrounding areas was significantly and negatively related to the percentage ungulates and primates sold in markets and significantly and positively related to the proportion of rodents. The proportion of carnivores sold was higher in markets with high human population densities. Proportion of small-bodied mammals (<1 kg) sold in markets increased as human population density increased, but proportion of large-bodied mammals (>10 kg) decreased as human population density increased. We calculated an index of game depletion (GDI) for each market from the sum of the total number of carcasses traded per annum and species, weighted by the intrinsic rate of natural increase (rmax ) of each species, divided by individuals traded in a market. The GDI of a market increased as the proportion of fast-reproducing species (highest rmax ) increased and as the representation of species with lowest rmax (slow-reproducing) decreased. The best explanatory factor for a market's GDI was anthropogenic pressure-road density, human settlements with >3000 inhabitants, and nonforest vegetation. High and low GDI were significantly differentiated by human density and human settlements with >3000 inhabitants. Our results provided empirical evidence that human activity is correlated with more depleted bushmeat faunas and can be used as a proxy to determine areas in need of conservation action.

Protected areas in tropical Africa: assessing threats and conservation activities.

Numerous protected areas (PAs) have been created in Africa to safeguard wildlife and other natural resources. However, significant threats from anthropogenic activities and decline of wildlife populations persist, while conservation efforts in most PAs are still minimal. We assessed the impact level of the most common threats to wildlife within PAs in tropical Africa and the relationship of conservation activities with threat impact level. We collated data on 98 PAs with tropical forest cover from 15 countries across West, Central and East Africa. For this, we assembled information about local threats as well as conservation activities from published and unpublished literature, and questionnaires sent to long-term field workers. We constructed general linear models to test the significance of specific conservation activities in relation to the threat impact level. Subsistence and commercial hunting were identified as the most common direct threats to wildlife and found to be most prevalent in West and Central Africa. Agriculture and logging represented the most common indirect threats, and were most prevalent in West Africa. We found that the long-term presence of conservation activities (such as law enforcement, research and tourism) was associated with lower threat impact levels. Our results highlight deficiencies in the management effectiveness of several PAs across tropical Africa, and conclude that PA management should invest more into conservation activities with long-term duration.

Mapping hotspots of threatened species traded in bushmeat markets in the Cross-Sanaga rivers region.

Bushmeat markets exist in many countries in West and Central Africa, and data on species sold can be used to detect patterns of wildlife trade in a region. We surveyed 89 markets within the Cross-Sanaga rivers region, West Africa. In each market, we counted the number of carcasses of each taxon sold. During a 6-month period (7594 market days), 44 mammal species were traded. Thirteen species were on the International Union for Conservation of Nature (IUCN) Red List or protected under national legislation, and at least 1 threatened species was traded in 88 of the 89 markets. We used these data to identify market groups that traded similar species assemblages. Using cluster analyses, we detected 8 market groups that were also geographically distinct. Market groups differed in the diversity of species, evenness of species, and dominant, prevalent, and characteristic species traded. We mapped the distribution of number of threatened species traded across the study region. Most threatened species were sold in markets nearest 2 national parks, Korup National Park in Cameroon and Cross River in Nigeria. To assess whether the threatened-species trade hotspots coincided with the known ranges of these species, we mapped the overlap of all threatened species traded. Markets selling more threatened species overlapped with those regions that had higher numbers of these. Our study can provide wildlife managers in the region with better tools to discern zones within which to focus policing efforts and reduce threats to species that are threatened by the bushmeat trade.