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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.
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Environment impacts gut microbiome richness in hybridizing chickadees, while ancestry influences community composition
Abstract Among closely related species, host phylogenetic relationships are typically a stronger predictor of gut microbiome composition than environmental variation. However, the relative impact of genetic admixture caused by hybridization versus environmental variation on gut microbiome communities is poorly understood. To explore this knowledge gap, we used fecal metabarcoding to characterize chickadee gut microbiomes along a hybrid zone transect in natural environments and after transfer to a common, controlled environment. We collected fecal samples from nestling black‐capped (Poecile atricapillus), Carolina (Poecile carolinensis), and hybrid chickadees immediately after removal from their nests and twice after entering captivity and experiencing common diet and environmental conditions. To characterize gut microbiome communities, we extracted fecal DNA and sequenced the V3–V4 region of the 16S rRNA gene using Illumina MiSeq. Overall,FirmicutesandProteobacteriawere the major microbial phyla present across host species groups. Our analysis of alpha diversity showed that the transition to common environmental conditions significantly impacted host gut microbiome richness. In contrast, the change in host environment did not impact the community composition (i.e., beta diversity) of the gut microbiomes. Although not statistically significant, host ancestry may influence the microbiome composition more than host environment. Additional analyses suggest chloroplast 16S rRNA sequences accurately characterized host diets in captivity. In certain cases, 16S rRNA sequences can provide reliable characterization of habitat and dietary variation in wild birds. Although environment more strongly shapes microbiome richness and evenness, host ancestry may have a greater influence on the specific microbes present in the microbiome.
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- PAR ID:
- 10677015
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Ecosphere
- Volume:
- 17
- Issue:
- 4
- ISSN:
- 2150-8925
- Page Range / eLocation ID:
- e70611
- Subject(s) / Keyword(s):
- Aves captivity gut symbionts microbial ecology microbiome hybridization
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/ecs2.70611
