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.

Changes in Grauer's gorilla (Gorilla beringei graueri) and other primate populations in the Kahuzi-Biega National Park and Oku Community Reserve, the heart of Grauer's gorilla global range.

Grauer's gorillas (Gorilla beringei graueri) have declined drastically across their range in eastern Democratic Republic of Congo (DRC). Survey data analysed in 2016 estimated a 77% decline in numbers between the mid- 1990s and 2016 and predicted that Kahuzi-Biega National Park (KBNP), and the contiguous Oku Community Reserve (OCR) held much of the global population. An estimate of 3800 Grauer's gorillas was made across its range at that time. Here, we publish the most extensive survey of Grauer's gorilla numbers to date, using nest counts from 230 line transects across KBNP and OCR to derive more accurate estimates of both gorilla and chimpanzee numbers. Gorilla numbers were estimated from line transects at 1,571 (95% confidence interval [CI]: 824-2,993) within KBNP and at 2,244 (95% CI: 1,471-3,422) in OCR. Eastern chimpanzee (Pan troglodytes schweinfurthii) numbers were estimated at 2,500 (95% CI: 1,804-3,462) in KBNP and 687 (95% CI: 472-999) in OCR. Estimates of total numbers for the survey area were 5,252 (95% CI: 3,687-7,481) Grauer's gorillas and 4,275 (95% CI: 3,322-5,502) eastern chimpanzees. Chimpanzee numbers were not significantly different from the estimates in the mid-1990s but the gorillas had significantly declined, mostly in KBNP. Modeled densities of these apes indicated that distances to mines, villages, or roads significantly explained part of the distribution of these apes, with higher densities also found in more rugged and remote sites. Other primates have all declined in this region, likely due to bushmeat hunting, especially the Endangered Ulindi River Red Colobus Piliocolobus lulindicus. These results confirm the negative impact of insecurity on Grauer's gorilla but indicate that the population declines may not be as great as previously feared. Using our revised gorilla density estimate we revise the original estimate of global numbers from 3,800 to 6,800 individuals.

Environmental variability supports chimpanzee behavioural diversity.

Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.

Cytomegalovirus distribution and evolution in hominines.

Herpesviruses are thought to have evolved in very close association with their hosts. This is notably the case for cytomegaloviruses (CMVs; genus Cytomegalovirus) infecting primates, which exhibit a strong signal of co-divergence with their hosts. Some herpesviruses are however known to have crossed species barriers. Based on a limited sampling of CMV diversity in the hominine (African great ape and human) lineage, we hypothesized that chimpanzees and gorillas might have mutually exchanged CMVs in the past. Here, we performed a comprehensive molecular screening of all 9 African great ape species/subspecies, using 675 fecal samples collected from wild animals. We identified CMVs in eight species/subspecies, notably generating the first CMV sequences from bonobos. We used this extended dataset to test competing hypotheses with various degrees of co-divergence/number of host switches while simultaneously estimating the dates of these events in a Bayesian framework. The model best supported by the data involved the transmission of a gorilla CMV to the panine (chimpanzee and bonobo) lineage and the transmission of a panine CMV to the gorilla lineage prior to the divergence of chimpanzees and bonobos, more than 800,000 years ago. Panine CMVs then co-diverged with their hosts. These results add to a growing body of evidence suggesting that viruses with a double-stranded DNA genome (including other herpesviruses, adenoviruses, and papillomaviruses) often jumped between hominine lineages over the last few million years.

Human impact erodes chimpanzee behavioral diversity.

Chimpanzees possess a large number of behavioral and cultural traits among nonhuman species. The "disturbance hypothesis" predicts that human impact depletes resources and disrupts social learning processes necessary for behavioral and cultural transmission. We used a dataset of 144 chimpanzee communities, with information on 31 behaviors, to show that chimpanzees inhabiting areas with high human impact have a mean probability of occurrence reduced by 88%, across all behaviors, compared to low-impact areas. This behavioral diversity loss was evident irrespective of the grouping or categorization of behaviors. Therefore, human impact may not only be associated with the loss of populations and genetic diversity, but also affects how animals behave. Our results support the view that "culturally significant units" should be integrated into wildlife conservation.

Catastrophic Decline of World's Largest Primate: 80% Loss of Grauer's Gorilla (Gorilla beringei graueri) Population Justifies Critically Endangered Status.

Grauer's gorilla (Gorilla beringei graueri), the World's largest primate, is confined to eastern Democratic Republic of Congo (DRC) and is threatened by civil war and insecurity. During the war, armed groups in mining camps relied on hunting bushmeat, including gorillas. Insecurity and the presence of several militia groups across Grauer's gorilla's range made it very difficult to assess their population size. Here we use a novel method that enables rigorous assessment of local community and ranger-collected data on gorilla occupancy to evaluate the impacts of civil war on Grauer's gorilla, which prior to the war was estimated to number 16,900 individuals. We show that gorilla numbers in their stronghold of Kahuzi-Biega National Park have declined by 87%. Encounter rate data of gorilla nests at 10 sites across its range indicate declines of 82-100% at six of these sites. Spatial occupancy analysis identifies three key areas as the most critical sites for the remaining populations of this ape and that the range of this taxon is around 19,700 km2. We estimate that only 3,800 Grauer's gorillas remain in the wild, a 77% decline in one generation, justifying its elevation to Critically Endangered status on the IUCN Red List of Threatened Species.

Assessing Host-Virus Codivergence for Close Relatives of Merkel Cell Polyomavirus Infecting African Great Apes.

UNLABELLED: It has long been hypothesized that polyomaviruses (PyV; family Polyomaviridae) codiverged with their animal hosts. In contrast, recent analyses suggested that codivergence may only marginally influence the evolution of PyV. We reassess this question by focusing on a single lineage of PyV infecting hominine hosts, the Merkel cell polyomavirus (MCPyV) lineage. By characterizing the genetic diversity of these viruses in seven African great ape taxa, we show that they exhibit very strong host specificity. Reconciliation analyses identify more codivergence than noncodivergence events. In addition, we find that a number of host and PyV divergence events are synchronous. Collectively, our results support codivergence as the dominant process at play during the evolution of the MCPyV lineage. More generally, our results add to the growing body of evidence suggesting an ancient and stable association of PyV and their animal hosts. IMPORTANCE: The processes involved in viral evolution and the interaction of viruses with their hosts are of great scientific interest and public health relevance. It has long been thought that the genetic diversity of double-stranded DNA viruses was generated over long periods of time, similar to typical host evolutionary timescales. This was also hypothesized for polyomaviruses (family Polyomaviridae), a group comprising several human pathogens, but this remains a point of controversy. Here, we investigate this question by focusing on a single lineage of polyomaviruses that infect both humans and their closest relatives, the African great apes. We show that these viruses exhibit considerable host specificity and that their evolution largely mirrors that of their hosts, suggesting that codivergence with their hosts played a major role in their diversification. Our results provide statistical evidence in favor of an association of polyomaviruses and their hosts over millions of years.

Chimpanzee accumulative stone throwing.

The study of the archaeological remains of fossil hominins must rely on reconstructions to elucidate the behaviour that may have resulted in particular stone tools and their accumulation. Comparatively, stone tool use among living primates has illuminated behaviours that are also amenable to archaeological examination, permitting direct observations of the behaviour leading to artefacts and their assemblages to be incorporated. Here, we describe newly discovered stone tool-use behaviour and stone accumulation sites in wild chimpanzees reminiscent of human cairns. In addition to data from 17 mid- to long-term chimpanzee research sites, we sampled a further 34 Pan troglodytes communities. We found four populations in West Africa where chimpanzees habitually bang and throw rocks against trees, or toss them into tree cavities, resulting in conspicuous stone accumulations at these sites. This represents the first record of repeated observations of individual chimpanzees exhibiting stone tool use for a purpose other than extractive foraging at what appear to be targeted trees. The ritualized behavioural display and collection of artefacts at particular locations observed in chimpanzee accumulative stone throwing may have implications for the inferences that can be drawn from archaeological stone assemblages and the origins of ritual sites.

Phylogenomic evidence for recombination of adenoviruses in wild gorillas.

Human adenoviruses (HAdVs) of species Human mastadenovirus B (HAdV-B) are genetically highly diverse and comprise several pathogenic types. AdVs closely related to members of HAdV-B infect African great apes and the evolutionary origin of HAdV-B has recently been determined in ancient gorillas. Genetic evidence for intra- and inter-species recombination has been obtained for AdVs of humans and captive great apes, but evidence from wild great apes is lacking. In this study, potential HAdV-B members of wild Eastern gorillas were analysed for evidence of recombination. One near-complete genome was amplified from primary sample material and sequenced, and from another six individuals genome fragments were obtained. In phylogenomic analysis, their penton base, pVII-pVI, hexon and fiber genes were compared with those of all publicly available HAdV-B full-genome sequences of humans and captive great apes. Evidence for intra-species recombination between different HAdV-B members of wild gorillas as well as between HAdV-B members of chimpanzees and gorillas was obtained. Since zoonotic AdVs have been reported to cause respiratory outbreaks in both humans and monkeys, and humans in West and Central Africa frequently hunt and butcher primates thereby increasing the chance of zoonotic transmission, such HAdV-B recombinants might widen the pool of potential human pathogens.

One or two species? On the case of Hyperolius discodactylus Ahl, 1931 and H. alticola Ahl, 1931 (Anura: Hyperoliidae).

In 1931, Ernst Ahl described two species of reed frogs inhabiting montane forests of the Albertine Rift in East Africa, Hyperolius alticola and H. discodactylus, which were synonymized two decades later by Raymond Laurent. Since then, this revision has been questioned repeatedly, but taxonomists have been reluctant to make a conclusive decision on the matter, especially since the type material of H. alticola was reported as being lost. Here, we examine the rediscovered type material of H. alticola and reassess the validity of Laurent's synonymy using morphological data from historic and new collections including all available type material, call recordings and molecular data from animals collected on recent expeditions. We find evidence for a northern and southern genetic clade, a divide that is somewhat supported by diverging morphology as well. However, no distinction in advertisement calls could be recovered to support this split and both genetic and morphological differences between geographic units are marginal and not always congruent and thus more likely reflect population-level variation. We therefore conclude that H. alticola is not a valid taxon and should continue to be treated as a synonym of H. discodactylus. Finally, we also report on newly collected material from outside the species known range, with first records of this species from Burundi.

Devastating decline of forest elephants in central Africa.

African forest elephants- taxonomically and functionally unique-are being poached at accelerating rates, but we lack range-wide information on the repercussions. Analysis of the largest survey dataset ever assembled for forest elephants (80 foot-surveys; covering 13,000 km; 91,600 person-days of fieldwork) revealed that population size declined by ca. 62% between 2002-2011, and the taxon lost 30% of its geographical range. The population is now less than 10% of its potential size, occupying less than 25% of its potential range. High human population density, hunting intensity, absence of law enforcement, poor governance, and proximity to expanding infrastructure are the strongest predictors of decline. To save the remaining African forest elephants, illegal poaching for ivory and encroachment into core elephant habitat must be stopped. In addition, the international demand for ivory, which fuels illegal trade, must be dramatically reduced.