Investigating Lemur Microbiomes Across Scales and in Relation to Natural and Anthropogenic Variation

Abstract

The composition and function of mammalian gut microbiomes are shaped by complex endogenous and exogenous factors that present on evolutionary and proximate timescales. In the Anthropocene era, host-associated microbiota are inevitably, yet differentially, influenced by natural and anthropogenic factors that vary across individuals and populations. In this dissertation, I used descriptive and experimental approaches, largely within a single species, the ring-tailed lemur (Lemur catta), to probe the roles of host physiology, environmental conditions, anthropogenic perturbation, and microbial environment in shaping primate microbiota across scales. First, I conducted a broad investigation of ring-tailed lemur gut microbiota and soil microbiota across 13 lemur populations (n = 209 individuals) spanning this species’ natural range in Madagascar, as well as multiple captivity settings in Madagascar and the U.S. By analyzing the lemur and soil microbiota, I showed that lemur gut microbiota vary widely within and between wild and captive populations, and that lemur and soil microbiota covary, suggesting a role for environmental acquisition in shaping interpopulation variation. Second, I analyzed vaginal, labial, and axillary microbiota of female ring-tailed lemurs and Coquerel’s sifakas (Propithecus coquereli) at the Duke Lemur Center (DLC) to demonstrate the influences of stable traits (e.g., species identity and mating system) and transient traits (e.g., ovarian hormones and forest access). We found that the effects of transient traits build on underlying differences mediated by stable traits. Third, and further focusing on DLC lemurs, but with a concentration on anthropogenic influence, I worked with a team of researchers to perform an experimental manipulation in ring-tailed lemurs to determine the influence of antibiotic treatment, with or without subsequent fecal transfaunation, on lemur gut microbiomes. I applied ecological frameworks to show that different facets of lemur microbial communities, such as bacterial diversity and composition, followed different recovery trajectories following antibiotic treatment. Fourth, I expanded my focus back to multiple ring-tailed lemur populations in natural and captivity settings to investigate the links between anthropogenic disturbance and antibiotic resistance genes (ARGs). I analyzed ARGs in wild and captive lemurs and soil from their habitats to show that lemur ARGs were correlated with anthropogenic disturbance and covaried with soil ARGs; lemur resistomes reflects multiple routes of ARG enrichment, including via antibiotic treatment or environmental acquisition. Integrating across these four data chapters, my results reveal that (a) the foundations of lemur-associated microbiomes are structured according to broad environmental conditions (e.g., wild vs. captive populations), but that between and within these broad categories, lemur microbiota are sensitive to more nuanced environmental variation, (b) lemur microbiota and resistomes co-vary with environmental microbiota, demonstrating the potential role of environmental acquisition in shaping host-associated communities across varying environments, and (c) integrating host microbial data across scales (e.g., at the individual and population level) with data on multiple facets of microbial communities (e.g., diversity, composition, membership, and resistomes), was key to providing a holistic perspective on host-associated and environmental microbe interactions across different microbial landscapes.