The One Health paradigm improves preventative medicine by understanding the effect of shared environments on human and animal health. Most studies under this paradigm have focused on pathogens shared between animals and humans. One Health research should also aim to measure non-pathogenic disease determinants shared within polyspecific communities. The network connecting primate population density, genetic diversity, and chronic health is nuanced, and human landscape modification affects those factors.
My research applies genetic and genomic methods to better understand how environmental factors may affect polyspecific primate community health.
Ecotoxicogenomics in a Monkey Model
Chlorocebus pygerythrus (vervet monkeys) thrive in anthropogenic habitats. Because they are a “least concern” taxon, they are an excellent model system to identify physiological responses to specific anthropogenic factors. My primary postdoctoral research program monitors the health, development, and genetics of two free-ranging populations of vervets in South Africa - one living in a protected reserve and the other on a private farm. Together with BU undergraduate mentees, Stacy-Anne Parke and Morgan Farrar, I found that farm-dwelling monkeys reach reproductive onset at an earlier age. Accelerated development in synanthropic monkeys may be due to increased caloric intake via nutritional provisioning on a farm, but differential toxicological factors also may alter developmental trajectories between habitat types. In a collaboration between Boston University, the University of Wisconsin Milwaukee, and the University of the Free State, I am quantifying anthropogenic endocrine disrupting chemicals (EDCs) (e.g., organophosphates, plasticizers) from both vervet habitats. EDCs can act as estrogens and antiestrogens by binding to estrogen receptors (ER⍺, ERβ). As transcription factors, ER⍺ and ERβ control expression of a cascade of genes essential for controlling growth, fertility and other functions. I will measure the effect of EDCs on the expression of ESR1 (the gene for ER⍺) and other genes under ER⍺’s control, mainly via RNA sequencing and real-time qPCR. Inhibition of ER⍺ reduces or prevents reproductive output in mouse models, so I will use behavioral and hormonal data collected from the vervets to measure the effect of EDC-ER⍺ interactions on copulatory behavior, fertility, and fecundity.
Chimpanzee Population Genetics and Health
While my current postdoctoral work emphasizes vervet monkeys as a model to understand chronic health, my broader research program tackles these questions using a wide taxonomic range of captive and wild primates, emphasizing health dynamics in primate communities. I studied the savanna chimpanzees at Toro-Semliki Wildlife Reserve in Uganda for my dissertation. Most of what we know about chimpanzees come from long-term studies at closed-forest sites, but at some savanna sites, the environment has selected for unique adaptations, such as lower population densities and larger home ranges. I used genetic capture-mark-recapture to estimate a surprisingly large population of ~187 individuals and found that they probably belong to a single community.
Toro-Semliki is compelling because of its savanna-designation, but also because it is one of four protected areas that serve as a transboundary “gateway” to connect the eastern chimpanzee subspecies’ stronghold in the DRC to neighboring Uganda. My study of mitochondrial DNA, which integrated my samples from Toro-Semliki with published sequences from across East Africa supports that designation. These results also suggest that the large population spans two protected areas: Toro-Semliki and neighboring Itwara Forest Reserve. If that is the case, it complicates the theoretically hard evolutionary line between “savanna” and “closed-forest” chimpanzees. Those results were presented this year at the Meetings of the International Primatological Society as an invited podium in the symposium Understanding Savanna Chimpanzees, where I also presented a study published in the Journal of Medical Primatology (2018). In that study, I found a surprisingly high incidence of testicular dysgenesis syndrome (TDS) among the Toro-Semliki chimpanzees that could not be explained by genetic drift.9 Instead, I proposed that environmental endocrine disruption is a likely culprit.
Variation in External Genitalia of Female Primates
That study of extreme variation in external genital morphology of wild male primates also inspired a current project involving external genitalia of wild female vervet monkeys in South Africa. Females at both of my study sites in South Africa presented with extreme variation in external genital morphology, including hypertrophied clitorises and male-pattern anal skin. Via qualitative photographic analysis, I found noticeable yet non-significant covariation with parity as well as covariation with life stage that approached significance. I presented that study with a call for standardized methods in quantifying variation of external genitalia in female primates at the Midwest Primate Interest Group this year.
Long-Term Research Site and Goals
My long-term goal is to apply my current work to the primate community at Itwara Forest Reserve. I carried out an initial pilot study (2017-2018) of the primate diversity in Itwara Forest Reserve (in prep, Oryx) via a series of reconnaissance surveys spanning corridors, edges, and central forest regions, while opportunistically collecting chimpanzee fecal samples for DNA analysis. I erected six Reconyx PC800 Hyperfire Professional Grade Camera Traps between March and September 2018 for a total of 6 months.
Initial image analysis shows the presence of chimpanzees, red-tailed monkeys (Cercopithecus ascanius), olive baboons (Papio anubis), pottos (Perodicticus ibeanus), black and white colobus monkeys (Colobus guereza) and blue monkeys (Cercopithecus mitis). Also, we captured images of non-primate conservation flagship mammals such as tree pangolins (Phataginus tricuspis), golden cats (Caracal aurata), leopards (Panthera pardus), and blue duikers (Philantomba monticola). My undergraduate mentee, Alyssa Lai, is cataloging these photos so that we can (1) assess general biodiversity and primate activity in each habitat type, (2) survey presence and temporal activity patterns of primate predators, and (3) examine the terrestriality of typically arboreal species (i.e., pottos) in the direct absence of humans. To better assess environmental disease determinants, I also conducted toxicological passive air sampling in each habitat type for five months in collaboration with Richard Mutageki of Makerere University and Tessa Steiniche at Indiana University. Analyses of these data are ongoing.
I look forward to returning to Itwara for more intensive sampling to initiate a long-term, novel engagement with the One Health paradigm on a polyspecific primate community by pioneering noninvasive methods in next-generation sequencing. My research on the interplay between shared environments, gene expression, and physiology currently relies on blood transcriptomes, which are often difficult or impossible to obtain from endangered, wild primates. That is why I am investigating alternative RNA sequencing options using noninvasive samples. Feces, for example, contain host epithelial cells with transcriptomes, and the biomedical literature contains successful examples of epithelial transcriptome sequencing. Through my collaborations at Wake Forest, I will pilot this method in captive vervet monkeys and then apply those techniques to the primate community at Itwara. With those results, I will then quantify the effect of anthropogenic toxins on gut pathology across different sympatric primate species. I will also investigate other noninvasive means of gathering transcriptome-quality samples, such as the use of hair traps to gather skin cells.