Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations

We acknowledge Royal Zoological Society of Scotland for providing core funding to BCFS and Leakey Foundation (R.M.W., C.C., T.D., K.Z.), British Academy (C.C.), Leverhulme Trust (K.Z.) and Max Planck Society (R.M.W., C.C. and T.D.) for funding the research.Stress is a major cause of poor health and mortality in humans and other social mammals. Close social bonds buffer stress, however much of the underlying physiological mechanism remains unknown. Here, we test two key hypotheses: bond partner effects occur only during stress (social buffering) or generally throughout daily life (main effects). We assess urinary glucocorticoids (uGC) in wild chimpanzees, with or without their bond partners, after a natural stressor, resting or everyday affiliation. Chimpanzees in the presence of, or interacting with, bond partners rather than others have lowered uGC levels across all three contexts. These results support the main effects hypothesis and indicate that hypothalamic-pituitary-adrenocortical (HPA) axis regulation is mediated by daily engagement with bond partners both within and out of stressful contexts. Regular social support with bond partners could lead to better health through daily ‘micro-management’ of the HPA axis, a finding with potential medical implications for humans.Publisher PDFPeer reviewe

Fly-derived DNA and camera traps are complementary tools for assessing mammalian biodiversity

Background Metabarcoding of vertebrate DNA found in invertebrates (iDNA) represents a potentially powerful tool for monitoring biodiversity. Preliminary evidence suggests fly iDNA biodiversity assessments compare favorably with established approaches such as camera trapping or line transects. Aims and Methods To assess whether fly-derived iDNA is consistently useful for biodiversity monitoring across a diversity of ecosystems, we compared metabarcoding of the mitochondrial 16S gene of fly pool-derived iDNA (range = 49–105 flies/site, N = 784 flies) with camera traps (range = 198–1,654 videos of mammals identified to the species level/site) at eight sites, representing different habitat types in five countries across tropical Africa. Results We detected a similar number of mammal species using fly-derived iDNA (range = 8–15 species/site) and camera traps (range = 8–27 species/site). However, the two approaches detected mostly different species (range = 6%–43% of species detected/site were detected with both methods), with fly-derived iDNA detecting on average smaller-bodied species than camera traps. Despite addressing different phylogenetic components of local mammalian communities, both methods resulted in similar beta-diversity estimates across sites and habitats. Conclusion These results support a growing body of evidence that fly-derived iDNA is a cost- and time-efficient tool that complements camera trapping in assessing mammalian biodiversity. Fly-derived iDNA may facilitate biomonitoring in terrestrial ecosystems at broad spatial and temporal scales, in much the same way as water eDNA has improved biomonitoring across aquatic ecosystems.Peer Reviewe

Generation Times in Wild Chimpanzees and Gorillas Suggest Earlier Divergence Times in Great Ape and Human Evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.Human Evolutionary Biolog

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

The Genetic Signature of Sex-Biased Migration in Patrilocal Chimpanzees and Humans

A large body of theoretical work suggests that analyses of variation at the maternally inherited mitochondrial (mt)DNA and the paternally inherited non-recombining portion of the Y chromosome (NRY) are a potentially powerful way to reveal the differing migratory histories of men and women across human societies. However, the few empirical studies comparing mtDNA and NRY variation and known patterns of sex-biased migration have produced conflicting results. Here we review some methodological reasons for these inconsistencies, and take them into account to provide an unbiased characterization of mtDNA and NRY variation in chimpanzees, one of the few mammalian taxa where males routinely remain in and females typically disperse from their natal groups. We show that patterns of mtDNA and NRY variation are more strongly contrasting in patrilocal chimpanzees compared with patrilocal human societies. The chimpanzee data we present here thus provide a valuable comparative benchmark of the patterns of mtDNA and NRY variation to be expected in a society with extremely female-biased dispersal

Population dynamics and genetic connectivity in recent chimpanzee history

The European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 864203) (to T.M.-B.). BFU2017-86471-P (MINECO/FEDER, UE) (to T.M.-B.). “Unidad de Excelencia María de Maeztu”, funded by the AEI (CEX2018-000792-M) (to T.M.-B.). Howard Hughes International Early Career (to T.M.-B.). NIH 1R01HG010898-01A1 (to T.M.-B.). Secretaria d’Universitats i Recerca and CERCA Program del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880) (to T.M.-B.). UCL’s Wellcome Trust ISSF3 award 204841/Z/16/Z (to A.M.A. and J.M.S.). Generalitat de Catalunya (2017 SGR-1040) (to M. Llorente). Wellcome Trust Investigator Award 202802/Z/16/Z (to D.A.H.). The Pan African Program: The Cultured Chimpanzee (PanAf) is generously funded by the Max Planck Society, the Max Planck Society Innovation Fund, and the Heinz L. Krekeler Foundation.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.Publisher PDFPeer reviewe

Author Correction: Environmental variability supports chimpanzee behavioural diversity

A Correction to this paper has been published: https://doi.org/10.1038/s41467-021-21010-z

Environmental variability supports chimpanzee behavioural diversity.

Funder: Max-Planck-Gesellschaft (Max Planck Society); doi: https://doi.org/10.13039/501100004189Funder: Heinz L. Krekeler FoundationLarge 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

Recent genetic connectivity and clinal variation in chimpanzees.

Funder: Max-Planck-Gesellschaft (Max Planck Society); doi: https://doi.org/10.13039/501100004189Funder: Max Planck Society Innovation Fund Heinz L. Krekeler FoundationMuch 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

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