Evidence of selection in the uncoupling protein 1 gene region suggests local adaptation to solar irradiance in savannah monkeys (Chlorocebus spp.).

In the last 300 thousand years, the genus Chlorocebus expanded from equatorial Africa into the southernmost latitudes of the continent, where colder climate was a probable driver of natural selection. We investigated population-level genetic variation in the mitochondrial uncoupling protein 1 (UCP1) gene region-implicated in non-shivering thermogenesis (NST)-in 73 wild savannah monkeys from three taxa representing this southern expansion (Chlorocebus pygerythrus hilgerti, Chlorocebus cynosuros and Chlorocebus pygerythrus pygerythrus) ranging from Kenya to South Africa. We found 17 single nucleotide polymorphisms with extended haplotype homozygosity consistent with positive selective sweeps, 10 of which show no significant linkage disequilibrium with each other. Phylogenetic generalized least-squares modelling with ecological covariates suggest that most derived allele frequencies are significantly associated with solar irradiance and winter precipitation, rather than overall low temperatures. This selection and association with irradiance is demonstrated by a relatively isolated population in the southern coastal belt of South Africa. We suggest that sunbathing behaviours common to savannah monkeys, in combination with the strength of solar irradiance, may mediate adaptations to thermal stress via NST among savannah monkeys. The variants we discovered all lie in non-coding regions, some with previously documented regulatory functions, calling for further validation and research.

Heavy metal ecotoxicology of vervet monkeys (Chlorocebus pygerythrus) across field sites in South Africa.

Primatologists use ecological models for understanding nonhuman primate (NHP) behavior and biology. Yet few studies have focused on the impacts of naturally occurring and anthropogenically derived toxicants in NHP habitats. For humans and NHPs, toxic levels of heavy metals frequently result in poor health outcomes including improper neurological development, immune system depression, and endocrine disruption. We analyzed the concentrations of lead (Pb), arsenic (As), and cadmium (Cd) in 48 vervet monkey (Chlorocebus pygerythrus) hair samples collected from eight South African groups living in environments with varying degrees of anthropogenic disturbance. We used two systems to categorize anthropogenic disturbance. The first was based on behavioral observations, home range overlap with human modified environments, and interviews with local people. The second system used stable isotope analysis (mean δ13C and δ15N hair values) from each group to estimate the consumption of C4 resources and the utilization of anthropogenically disturbed habitats. Preliminary analyses revealed differences in the Pb and As hair concentrations across the field sites (p < 0.05). Comparisons between anthropogenic disturbance using observations and interviews revealed differences in As (p < 0.01). In contrast, comparisons between categories using δ13C hair values revealed differences in Pb (p < 0.05). The results from this study suggest that multiple approaches using both qualitative and quantitative data should be employed to estimate the relationship between anthropogenic disturbance and environmental toxicants. Since many NHP populations share their habitats with humans, efforts to improve these landscapes would likely be beneficial for NHP and human health.

Shifts in microbial diversity, composition, and functionality in the gut and genital microbiome during a natural SIV infection in vervet monkeys.

BACKGROUND: The microbiota plays an important role in HIV pathogenesis in humans. Microbiota can impact health through several pathways such as increasing inflammation in the gut, metabolites of bacterial origin, and microbial translocation from the gut to the periphery which contributes to systemic chronic inflammation and immune activation and the development of AIDS. Unlike HIV-infected humans, SIV-infected vervet monkeys do not experience gut dysfunction, microbial translocation, and chronic immune activation and do not progress to immunodeficiency. Here, we provide the first reported characterization of the microbial ecosystems of the gut and genital tract in a natural nonprogressing host of SIV, wild vervet monkeys from South Africa. RESULTS: We characterized fecal, rectal, vaginal, and penile microbiomes in vervets from populations heavily infected with SIV from diverse locations across South Africa. Geographic site, age, and sex affected the vervet microbiome across different body sites. Fecal and vaginal microbiome showed marked stratification with three enterotypes in fecal samples and two vagitypes, which were predicted functionally distinct within each body site. External bioclimatic factors, biome type, and environmental temperature influenced microbiomes locally associated with vaginal and rectal mucosa. Several fecal microbial taxa were linked to plasma levels of immune molecules, for example, MIG was positively correlated with Lactobacillus and Escherichia/Shigella and Helicobacter, and IL-10 was negatively associated with Erysipelotrichaceae, Anaerostipes, Prevotella, and Anaerovibrio, and positively correlated with Bacteroidetes and Succinivibrio. During the chronic phase of infection, we observed a significant increase in gut microbial diversity, alterations in community composition (including a decrease in Proteobacteria/Succinivibrio in the gut) and functionality (including a decrease in genes involved in bacterial invasion of epithelial cells in the gut), and partial reversibility of acute infection-related shifts in microbial abundance observed in the fecal microbiome. As part of our study, we also developed an accurate predictor of SIV infection using fecal samples. CONCLUSIONS: The vervets infected with SIV and humans infected with HIV differ in microbial responses to infection. These responses to SIV infection may aid in preventing microbial translocation and subsequent disease progression in vervets, and may represent host microbiome adaptations to the virus. Video Abstract.

ACE2 and TMPRSS2 variation in savanna monkeys (Chlorocebus spp.): Potential risk for zoonotic/anthroponotic transmission of SARS-CoV-2 and a potential model for functional studies.

The COVID-19 pandemic, caused by the coronavirus SARS-CoV-2, has devastated health infrastructure around the world. Both ACE2 (an entry receptor) and TMPRSS2 (used by the virus for spike protein priming) are key proteins to SARS-CoV-2 cell entry, enabling progression to COVID-19 in humans. Comparative genomic research into critical ACE2 binding sites, associated with the spike receptor binding domain, has suggested that African and Asian primates may also be susceptible to disease from SARS-CoV-2 infection. Savanna monkeys (Chlorocebus spp.) are a widespread non-human primate with well-established potential as a bi-directional zoonotic/anthroponotic agent due to high levels of human interaction throughout their range in sub-Saharan Africa and the Caribbean. To characterize potential functional variation in savanna monkey ACE2 and TMPRSS2, we inspected recently published genomic data from 245 savanna monkeys, including 163 wild monkeys from Africa and the Caribbean and 82 captive monkeys from the Vervet Research Colony (VRC). We found several missense variants. One missense variant in ACE2 (X:14,077,550; Asp30Gly), common in Ch. sabaeus, causes a change in amino acid residue that has been inferred to reduce binding efficiency of SARS-CoV-2, suggesting potentially reduced susceptibility. The remaining populations appear as susceptible as humans, based on these criteria for receptor usage. All missense variants observed in wild Ch. sabaeus populations are also present in the VRC, along with two splice acceptor variants (at X:14,065,076) not observed in the wild sample that are potentially disruptive to ACE2 function. The presence of these variants in the VRC suggests a promising model for SARS-CoV-2 infection and vaccine and therapy development. In keeping with a One Health approach, characterizing actual susceptibility and potential for bi-directional zoonotic/anthroponotic transfer in savanna monkey populations may be an important consideration for controlling COVID-19 epidemics in communities with frequent human/non-human primate interactions that, in many cases, may have limited health infrastructure.

Publisher Correction: Ancient hybridization and strong adaptation to viruses across African vervet monkey populations.

In the version of this article published, in the Online Methods eight citations to supplementary material refer to the wrong supplementary items. See the correction notice for full details.

Adaptive genetic variation at three loci in South African vervet monkeys (Chlorocebus pygerythrus) and the role of selection within primates.

Vervet monkeys (Chlorocebus pygerythrus) are one of the most widely distributed non-human primate species found in South Africa. They occur across all the South African provinces, inhabiting a large variety of habitats. These habitats vary sufficiently that it can be assumed that various factors such as pathogen diversity could influence populations in different ways. In turn, these factors could lead to varied levels of selection at specific fitness linked loci. The Toll-like receptor (TLR) gene family, which play an integral role in vertebrate innate immunity, is a group of fitness linked loci which has been the focus of much research. In this study, we assessed the level of genetic variation at partial sequences of two TLR loci (TLR4 and 7) and a reproductively linked gene, acrosin (ACR), across the different habitat types within the vervet monkey distribution range. Gene variation and selection estimates were also made among 11-21 primate species. Low levels of genetic variation for all three gene regions were observed within vervet monkeys, with only two polymorphic sites identified for TLR4, three sites for TLR7 and one site for ACR. TLR7 variation was positively correlated with high mean annual rainfall, which was linked to increased pathogen abundance. The observed genetic variation at TLR4 might have been influenced by numerous factors including pathogens and climatic conditions. The ACR exonic regions showed no variation in vervet monkeys, which could point to the occurrence of a selective sweep. The TLR4 and TLR7 results for the among primate analyses was mostly in line with previous studies, indicating a higher rate of evolution for TLR4. Within primates, ACR coding regions also showed signs of positive selection, which was congruent with previous reports on mammals. Important additional information to the already existing vervet monkey knowledge base was gained from this study, which can guide future research projects on this highly researched taxon as well as help conservation agencies with future management planning involving possible translocations of this species.

Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth.

OBJECTIVES: Direct comparative work in morphology and growth on widely dispersed wild primate taxa is rarely accomplished, yet critical to understanding ecogeographic variation, plastic local variation in response to human impacts, and variation in patterns of growth and sexual dimorphism. We investigated population variation in morphology and growth in response to geographic variables (i.e., latitude, altitude), climatic variables (i.e., temperature and rainfall), and human impacts in the vervet monkey (Chlorocebus spp.). METHODS: We trapped over 1,600 wild vervets from across Sub-Saharan Africa and the Caribbean, and compared measurements of body mass, body length, and relative thigh, leg, and foot length in four well-represented geographic samples: Ethiopia, Kenya, South Africa, and St. Kitts & Nevis. RESULTS: We found significant variation in body mass and length consistent with Bergmann's Rule in adult females, and in adult males when excluding the St. Kitts & Nevis population, which was more sexually dimorphic. Contrary to Rensch's Rule, although the South African population had the largest average body size, it was the least dimorphic. There was significant, although very small, variation in all limb segments in support for Allen's Rule. Females in high human impact areas were heavier than those with moderate exposures, while those in low human impact areas were lighter; human impacts had no effect on males. CONCLUSIONS: Vervet monkeys appear to have adapted to local climate as predicted by Bergmann's and, less consistently, Allen's Rule, while also responding in predicted ways to human impacts. To better understand deviations from predicted patterns will require further comparative work in vervets.

Participation, representation, and shared experiences of women scholars in biological anthropology.

American Association of Physical Anthropologists (AAPA) membership surveys from 1996 and 1998 revealed significant gender disparities in academic status. A 2014 follow-up survey showed that gender equality had improved, particularly with respect to the number of women in tenure-stream positions. However, although women comprised 70% of AAPA membership at that time, the percentage of women full professors remained low. Here, we continue to consider the status of women in biological anthropology by examining the representation of women through a quantitative analysis of their participation in annual meetings of the AAPA during the past 20 years. We also review the programmatic goals of the AAPA Committee on Diversity Women's Initiative (COD-WIN) and provide survey results of women who participated in COD-WIN professional development workshops. Finally, we examine the diversity of women's career paths through the personal narratives of 14 women biological anthropologists spanning all ranks from graduate student to Professor Emeritus. We find that over the past 20 years, the percentage of women first authors of invited symposia talks has increased, particularly in the sub-disciplines of bioarchaeology, genetics, and paleoanthropology. The percentage of women first authors on contributed talks and posters has also increased. However, these observed increases are still lower than expected given the percentage of graduate student women and women at the rank of assistant and associate professor. The personal narratives highlight first-hand the impact of mentoring on career trajectory, the challenges of achieving work-life satisfaction, and resilience in the face of the unexpected. We end with some suggestions for how to continue to improve equality and equity for women in biological anthropology.

Ancient hybridization and strong adaptation to viruses across African vervet monkey populations.

Vervet monkeys are among the most widely distributed nonhuman primates, show considerable phenotypic diversity, and have long been an important biomedical model for a variety of human diseases and in vaccine research. Using whole-genome sequencing data from 163 vervets sampled from across Africa and the Caribbean, we find high diversity within and between taxa and clear evidence that taxonomic divergence was reticulate rather than following a simple branching pattern. A scan for diversifying selection across taxa identifies strong and highly polygenic selection signals affecting viral processes. Furthermore, selection scores are elevated in genes whose human orthologs interact with HIV and in genes that show a response to experimental simian immunodeficiency virus (SIV) infection in vervet monkeys but not in rhesus macaques, suggesting that part of the signal reflects taxon-specific adaptation to SIV.

Transmission of Staphylococcus aureus from Humans to Green Monkeys in The Gambia as Revealed by Whole-Genome Sequencing.

UNLABELLED: Staphylococcus aureus is an important pathogen of humans and animals. We genome sequenced 90 S. aureus isolates from The Gambia: 46 isolates from invasive disease in humans, 13 human carriage isolates, and 31 monkey carriage isolates. We inferred multiple anthroponotic transmissions of S. aureus from humans to green monkeys (Chlorocebus sabaeus) in The Gambia over different time scales. We report a novel monkey-associated clade of S. aureus that emerged from a human-to-monkey switch estimated to have occurred 2,700 years ago. Adaptation of this lineage to the monkey host is accompanied by the loss of phage-carrying genes that are known to play an important role in human colonization. We also report recent anthroponotic transmission of the well-characterized human lineages sequence type 6 (ST6) and ST15 to monkeys, probably because of steadily increasing encroachment of humans into the monkeys' habitat. Although we have found no evidence of transmission of S. aureus from monkeys to humans, as the two species come into ever-closer contact, there might be an increased risk of additional interspecies exchanges of potential pathogens. IMPORTANCE: The population structures of Staphylococcus aureus in humans and monkeys in sub-Saharan Africa have been previously described using multilocus sequence typing (MLST). However, these data lack the power to accurately infer details regarding the origin and maintenance of new adaptive lineages. Here, we describe the use of whole-genome sequencing to detect transmission of S. aureus between humans and nonhuman primates and to document the genetic changes accompanying host adaptation. We note that human-to-monkey switches tend to be more common than the reverse and that a novel monkey-associated clade is likely to have emerged from such a switch approximately 2,700 years ago. Moreover, analysis of the accessory genome provides important clues as to the genetic changes underpinning host adaptation and, in particular, shows that human-to-monkey switches tend to be associated with the loss of genes known to confer adaptation to the human host.

Morphological variation in Homo erectus and the origins of developmental plasticity.

Homo erectus was the first hominin to exhibit extensive range expansion. This extraordinary departure from Africa, especially into more temperate climates of Eurasia, has been variously related to technological, energetic and foraging shifts. The temporal and regional anatomical variation in H. erectus suggests that a high level of developmental plasticity, a key factor in the ability of H. sapiens to occupy a variety of habitats, may also have been present in H. erectus. Developmental plasticity, the ability to modify development in response to environmental conditions, results in differences in size, shape and dimorphism across populations that relate in part to levels of resource sufficiency and extrinsic mortality. These differences predict not only regional variations but also overall smaller adult sizes and lower levels of dimorphism in instances of resource scarcity and high predator load. We consider the metric variation in 35 human and non-human primate 'populations' from known environmental contexts and 14 time- and space-restricted paleodemes of H. erectus and other fossil Homo Human and non-human primates exhibit more similar patterns of variation than expected, with plasticity evident, but in differing patterns by sex across populations. The fossil samples show less evidence of variation than expected, although H. erectus varies more than Neandertals.This article is part of the themed issue 'Major transitions in human evolution'.

A comparison of adult body size between captive and wild vervet monkeys (Chlorocebus aethiops sabaeus) on the island of St. Kitts.

Weight and 34 morphological measurements were obtained from 103 vervet monkeys living either in the wild or in captive colonies derived from the wild populations on the island of St. Kitts in the Eastern Caribbean. All measures were taken during the same week, eliminating bias that might result from changing seasonal environmental conditions. Vervets on St. Kitts are all descended from a small number of individuals brought to the island approximately 400 years ago from West Africa, thus eliminating bias that might result from subspecific size differences. We conducted a principal components analysis (PCA) and compared individual traits between captive and wild adult animals. Morphological measures such as body, arm, and leg length did not differ significantly between animals living in the wild and animals in captivity. Weight and measures indicating condition-including body mass index (BMI), chest, thigh, and upper arm girth were all higher for animals living in captivity. More consistent available food is probably the cause of differences in measures reflecting condition.

Localized population divergence of vervet monkeys (Chlorocebus spp.) in South Africa: Evidence from mtDNA.

OBJECTIVE: Vervet monkeys are common in most tree-rich areas of South Africa, but their absence from grassland and semi-desert areas of the country suggest potentially restricted and mosaic local population patterns that may have relevance to local phenotype patterns and selection. A portion of the mitochondrial DNA control region was sequenced to study patterns of genetic differentiation. METHODS: DNA was extracted, and mitochondrial DNA sequences were obtained from 101 vervet monkeys at 15 localities, which represent both an extensive (widely across the distribution range) and intensive (more than one troop at most of the localities) sampling strategy. Analyses utilized Arlequin 3.1, MEGA 6, BEAST v1.5.2, and Network V3.6.1. RESULTS: The dataset contained 26 distinct haplotypes, with six populations fixed for single haplotypes. Pairwise P-distance among population pairs showed significant differentiation among most population pairs, but with nonsignificant differences among populations within some regions. Populations were grouped into three broad clusters in a maximum likelihood phylogenetic tree and a haplotype network. These clusters correspond to i) north-western, northern, and north-eastern parts of the distribution range as well as the northern coastal belt; ii) central areas of the country; and iii) southern part of the Indian Ocean coastal belt and adjacent inland areas. CONCLUSIONS: Apparent patterns of genetic structure correspond to current and past distribution of suitable habitat, geographic barriers to gene flow, geographic distance, and female philopatry. However, further work on nuclear markers and other genomic data are necessary to confirm these results.