Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

Abstract

Background: Inter-population variation in host-associated microbiota reflects differences in the hosts' environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes - an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used source-sink ecological theory to examine covariation between the two types of consortia. Results: The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or condition. Variation in microbial composition was inconsistent with either a single, representative gut community for wild conspecifics or a universal 'signal of captivity' that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemurs within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities were most distinct between the two continents, and there was significant and context-specific covariation between lemur gut and soil microbiota. Conclusions: As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple 'captive vs. wild' dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.

Captive and urban environments are associated with distinct gut microbiota in deer mice ( Peromyscus maniculatus )

“…The distinct urban deer mice and similarity between captive populations lead to the result that environment type superseded any geographical effect on the gut microbiota. Geographical location has previously been shown to play a large role in shaping mammalian gut microbial composition [2,30], sometimes to the extent that it overcomes signals of environment type, as in a recent study of captive and wild lemurs [8]. The similarity of the two populations from undeveloped locations, located several states away, confirms the limited effect of geography in our study.…”

Antibiotic Resistance Genes in Lemur Gut and Soil Microbiota Along a Gradient of Anthropogenic Disturbance

“…With growing recognition that animal hosts represent only one component of microbial landscapes, researchers are increasingly probing the relationships between host-associated and environmental microbiota. In a previous study on these same ring-tailed lemur populations, we showed that exposure to and acquisition of soil microbes likely contributed to interpopulation variation in gut microbiota (Bornbusch et al, 2021). Here, we expand on this finding, showing that the same pattern holds for ARGs: significant covariation between lemur gut and soil resistomes was found in two disturbed sites, ISA and BEZ.…”

“…Although not directly addressed in the present study, one such pressure may involve host sociality. Notably, the sitespecificity we observed in lemur resistomes mirrors the siteor group-specificity observed for microbiome composition in highly social species (Theis et al, 2012;Leclaire et al, 2014;Tung et al, 2015;Moeller et al, 2016), including the ring-tailed lemur (Bornbusch et al, 2021). The widely accepted mechanism underlying these patterns is the sharing of microbes between hosts, from many possible bodily sources, particularly between conspecific social partners (reviewed in Archie and Tung, 2015).…”

“…The protocols associated with sample collection are detailed in Bornbusch et al, 2021. In brief, we opportunistically collected fresh fecal samples from lemurs at all 10 sites. We additionally collected soil samples from the lemurs' core areas at four of the natural habitat sites (Table 1).…”

Host Identity and Geographic Location Significantly Affect Gastrointestinal Microbial Richness and Diversity in Western Lowland Gorillas (Gorilla gorilla gorilla) under Human Care

“…Temperate regions have been documented to have seasonal turnover of soil microbial populations, specifically in Colorado forests [ 22 ]. Bornbusch et al [ 23 ] also found that lemur GI microbiomes displayed seasonal fluctuations under human care. Seasonal changes in wild gorilla GI microbiome composition were previously documented by Gomez et al [ 10 ], although these changes were thought to be primarily driven by dietary changes rather than environmental changes.…”