Recent genetic connectivity and clinal variation in chimpanzees.

Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

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.

Maximizing the acquisition of unique reads in noninvasive capture sequencing experiments.

Noninvasive samples as a source of DNA are gaining interest in genomic studies of endangered species. However, their complex nature and low endogenous DNA content hamper the recovery of good quality data. Target capture has become a productive method to enrich the endogenous fraction of noninvasive samples, such as faeces, but its sensitivity has not yet been extensively studied. Coping with faecal samples with an endogenous DNA content below 1% is a common problem when prior selection of samples from a large collection is not possible. However, samples classified as unfavourable for target capture sequencing might be the only representatives of unique specific geographical locations, or to answer the question of interest. To explore how library complexity may be increased without repeating DNA extractions and generating new libraries, in this study we captured the exome of 60 chimpanzees (Pan troglodytes) using faecal samples with very low proportions of endogenous content (<1%). Our results indicate that by performing additional hybridizations of the same libraries, the molecular complexity can be maintained to achieve higher coverage. Also, whenever possible, the starting DNA material for capture should be increased. Finally, we specifically calculated the sequencing effort needed to avoid exhausting the library complexity of enriched faecal samples with low endogenous DNA content. This study provides guidelines, schemes and tools for laboratories facing the challenges of working with noninvasive samples containing extremely low amounts of endogenous DNA.

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue.

Many non-human primate species in sub-Saharan Africa are infected with Treponema pallidum subsp. pertenue, the bacterium causing yaws in humans. In humans, yaws is often characterized by lesions of the extremities and face, while T. pallidum subsp. pallidum causes venereal syphilis and is typically characterized by primary lesions on the genital, anal or oral mucosae. It remains unclear whether other T. pallidum subspecies found in humans also occur in non-human primates and how the genomic diversity of non-human primate T. pallidum subsp. pertenue lineages is distributed across hosts and space. We observed orofacial and genital lesions in sooty mangabeys (Cercocebus atys) in Taï National Park, Côte d'Ivoire and collected swabs and biopsies from symptomatic animals. We also collected non-human primate bones from 8 species in Taï National Park and 16 species from 11 other sites across sub-Saharan Africa. Samples were screened for T. pallidum DNA using polymerase chain reactions (PCRs) and we used in-solution hybridization capture to sequence T. pallidum genomes. We generated three nearly complete T. pallidum genomes from biopsies and swabs and detected treponemal DNA in bones of six non-human primate species in five countries, allowing us to reconstruct three partial genomes. Phylogenomic analyses revealed that both orofacial and genital lesions in sooty mangabeys from Taï National Park were caused by T. pallidum subsp. pertenue. We showed that T. pallidum subsp. pertenue has infected non-human primates in Taï National Park for at least 28 years and has been present in two non-human primate species that had not been described as T. pallidum subsp. pertenue hosts in this ecosystem, western chimpanzees (Pan troglodytes verus) and western red colobus (Piliocolobus badius), complementing clinical evidence that started accumulating in Taï National Park in 2014. More broadly, simian T. pallidum subsp. pertenue strains did not form monophyletic clades based on host species or the symptoms caused, but rather clustered based on geography. Geographical clustering of T. pallidum subsp. pertenue genomes might be compatible with cross-species transmission of T. pallidum subsp. pertenue within ecosystems or environmental exposure, leading to the acquisition of closely related strains. Finally, we found no evidence for mutations that confer antimicrobial resistance.

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.

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.

Additive genetic variation for tolerance to estrogen pollution in natural populations of Alpine whitefish (Coregonus sp., Salmonidae).

The evolutionary potential of natural populations to adapt to anthropogenic threats critically depends on whether there exists additive genetic variation for tolerance to the threat. A major problem for water-dwelling organisms is chemical pollution, and among the most common pollutants is 17α-ethinylestradiol (EE2), the synthetic estrogen that is used in oral contraceptives and that can affect fish at various developmental stages, including embryogenesis. We tested whether there is variation in the tolerance to EE2 within Alpine whitefish. We sampled spawners from two species of different lakes, bred them in vitro in a full-factorial design each, and studied growth and mortality of embryos. Exposure to EE2 turned out to be toxic in all concentrations we tested (≥1 ng/L). It reduced embryo viability and slowed down embryogenesis. We found significant additive genetic variation in EE2-induced mortality in both species, that is, genotypes differed in their tolerance to estrogen pollution. We also found maternal effects on embryo development to be influenced by EE2, that is, some maternal sib groups were more susceptible to EE2 than others. In conclusion, the toxic effects of EE2 were strong, but both species demonstrated the kind of additive genetic variation that is necessary for an evolutionary response to this type of pollution.