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 microbial source tracking 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 environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between 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.

Anthropogenic Disturbance Impacts Gut Microbiome Homeostasis in a Malagasy Primate

“…We did not observe any effect of sex on both alpha and beta gut microbial diversity of mouse lemurs. Defining the role of sex in shaping lemur microbiomes is challenging since earlier studies provided mixed results, reporting either a significant role of sex ( Perofsky et al, 2021 ) or no sex-dependent effects ( Bornbusch et al, 2022 ).…”

Growing and maintaining a network for early career researchers through the Animal Microbiome Research Group

“…Dr. Sally Bornbusch (Smithsonian's National Zoo & Conservation Biology Institute, USA) emphasized that microbes can also be acquired from the environment by showing that wild ring-tailed lemurs harbored a greater relative abundance of soil-associated microbes than captiveenvironment conspecifics. 6 Thus, both social and environmental transmission can influence gut microbiome composition. This was reinforced by Dr. Aura Raulo (University of Turku, Finland), who reported that among wild wood mice, anaerobic taxa in the microbiome were linked to social patterns, while aerotolerant taxa underlay spatial patterns.…”

“…Jonas Torfs (University of Antwerp, Belgium) presented his PhD project on the microbiome‐gut‐brain axis in captive bonobos where he will investigate effects of grooming. Dr. Sally Bornbusch (Smithsonian's National Zoo & Conservation Biology Institute, USA) emphasized that microbes can also be acquired from the environment by showing that wild ring‐tailed lemurs harbored a greater relative abundance of soil‐associated microbes than captive‐environment conspecifics 6 . Thus, both social and environmental transmission can influence gut microbiome composition.…”

Assessing the causes and consequences of gut mycobiome variation in a wild vertebrate population

“…survival and reproductive success) in the wild. This is despite growing evidence that captivity can signi cantly alter, and in many cases simplify, the GM [26,27], including the mycobiome [23,28]. Wild animals are exposed to highly complex and dynamic environments which are very di cult to replicate in captivity, but which shape the GM and interact with host tness [29].…”