Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Rojas, Connie A.; Ramírez‐Barahona, Santiago; Holekamp, Kay E.; Theis, Kevin R.

doi:10.1101/2020.09.23.299727

Cited by 7 publications

(8 citation statements)

References 109 publications

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“…We observed considerable variations in the gut microbial composition at interspecific level despite sympatric distribution of rodents in Liaoning or Heilongjiang province. These observations were consistent with the results of previous studies showing a close correlation between the similarity of their microbial composition and the phylogenetic relationships of the hosts (Phillips et al, 2012;Mario et al, 2015;Brooks et al, 2016;Rojas et al, 2021). PCoA analyses found species identity significantly explained 20.9% of the Frontiers in Microbiology 07 frontiersin.org beta diversity between samples, which was much higher than that explained by geographic location.…”

Section: Discussionsupporting

confidence: 92%

“…Phylosymbiosis conveys the idea that genetic backgrounds of the host animals are closely related to changes in their gut microbial diversity (Brooks et al, 2016). However, host genetics and host ecology may structure the gut microbiota of mammals at different taxonomic scales (Rojas et al, 2021). Diet has been believed to be a crucial factor in structuring gut microbial diversity in the context of host ecology.…”

Section: Discussionmentioning

confidence: 99%

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The influence of species identity and geographic locations on gut microbiota of small rodents

Wang

Zhang

et al. 2022

Front. Microbiol.

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Although the correlation between gut microbiota, species identity and geographic locations has long attracted the interest of scientists, to what extent species identity and geographic locations influence the gut microbiota assemblages in granivorous rodents needs further investigation. In this study, we performed a survey of gut microbial communities of four rodent species (Apodemus agrarius, A. peninsulae, Tamias sibiricus and Clethrionomys rufocanus) distributed in two areas with great distance (> 600 km apart), to assess if species identity dominates over geographic locations in shaping gut microbial profiles using 16S rRNA gene sequencing. We found that gut microbiota composition varied significantly across host species and was closely correlated with host genetics. We identified strong species identity effects on gut microbial composition, with a comparatively weaker signal of geographic provenance on the intestinal microbiota. Specifically, microbiota of one species was on average more similar to that of conspecifics living in separate sites than to members of a closely related species living in the same location. Our study suggests that both host genetics and geographical variations influence gut microbial diversity of four rodent species, which merits further investigation to reveal the patterns of phylogenetic correlation of gut microbial community assembly in mammals across multiple habitats.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

The influence of species identity and geographic locations on gut microbiota of small rodents

Wang

Zhang

et al. 2022

Front. Microbiol.

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“…The gut microbiome is shaped by numerous factors including host evolutionary relationships, social interactions, habitat, and diet (Archie & Tung, 2015; Rojas et al, 2021; Youngblut et al, 2019). In wild animals, distinct populations living under different ecological conditions have frequently been shown to possess unique gut microbiomes (Bueno de Mesquita et al, 2021; Couch et al, 2020; Uren Webster et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…The gut microbiome is shaped by numerous factors including host evolutionary relationships, social interactions, habitat, and diet Rojas et al, 2021;Youngblut et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Isolated Grauer’s gorilla populations differ in diet and gut microbiome

Michel

Minocher

Niehoff

et al. 2022

Preprint

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Conservation efforts tend to focus on populations that are genetically differentiated without paying attention to their ecological differentiation. However, isolated populations may be ecologically unique, an important aspect for the design of appropriate conservation measures for endangered species. Here we investigate the interplay between diet and gut microbiome in several geographically isolated and genetically differentiated populations of the critically endangered Grauer's gorilla. We find that dietary and gut microbial profiles are population-specific, likely due to geographic isolation and environmental differences. In addition, social groups within each population also differed in diet and, to a lesser extent, in gut microbial composition and diversity. Individuals at low elevation consumed a larger variety of plant taxa than those at high elevation, consistent with the notion that dietary choice is constrained by food availability that changes with elevation. Despite no detectable correlation between the diet and gut microbiome in richness or evenness, dietary and gut microbial composition covaried significantly. As we did not find evidence for an effect of genetic relatedness on the composition of the gut microbiome of Grauer's gorillas, this pattern is likely a result of long-term social, ecological, and geographic factors acting on both diet and microbiome. These results reveal that isolated and genetically distinct populations of Grauer's gorillas are also ecologically distinct, highlighting the need to dedicate separate conservation efforts for each population.

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“…Collectively this indicates a critical role of the gut microbiota in forging the host ecology and influencing its evolutionary outcomes (Alberdi et al, 2016; Shapira, 2016). On the other hand, the gut microbiota structure itself is largely shaped by the host factors, including genotype, diet (Rojas et al, 2021; Youngblut et al, 2019), and geography (Levin et al, 2021), with results varying between captive and wild samples (Youngblut et al, 2019) and depending on the taxonomic scale of observation, both for microbes (from strain to phylum) and hosts (from individuals up to species and families) (Alberdi et al, 2021; Rojas et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Insular holobionts: persistence and seasonal plasticity of the Balearic wall lizard (Podarcis lilfordi) gut microbiota

Baldo

Tavecchia

Rotger

et al. 2022

Preprint

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Integrative studies of animals and associated microbial assemblages (i.e., the holobiont) are rapidly changing our perspectives on organismal ecology and evolution. Islands provide ideal natural systems to understand the biogeographic patterns that shape these symbiotic associations, their resilience and plasticity over temporal and spatial scales, and ultimately their role in the host ecological adaptation. Here we used the Balearic wall lizard Podarcis lilfordi to address the diversification of the holobiont in an insular context by dissecting the drivers of the gut microbiota diversity within and across host allopatric populations. By extensive fecal sampling of individually identified lizards from three closed populations/islets in the South of Mallorca (Na Moltona, Na Guardis and En Curt) along two years and two seasons (spring and autumn), we sorted out the effect of islet, year, season, sex and partly life stage on the microbiota composition. We further related microbiota distances to host genetics and trophic ecology. Overall, the three populations showed a remarkable conservation of the major microbial taxonomic profile, while carrying their unique microbial signature at finer level of taxonomic resolution (Amplicon Sequence Variants (ASVs)). Microbiota distances across populations were compatible with both host genetics (as inferred by microsatellites) and trophic niche distances (as inferred by stable isotopes and fecal content). Within populations, a large proportion of ASVs (30-50%) persisted along the four sampling dates. Microbial diversity was driven by life stage and season, with no annual or sex effect. Seasonal changes within islets were mainly associated with fluctuations in the relative abundances of few bacterial taxa (mostly families Lachnospiraceae and Ruminococcaceae), consistently in both sampled years and without any major compositional turnover. These results support a large resilience of the major compositional aspects of the P. lilfordi gut microbiota over the short-term evolutionary divergence of their host allopatric populations (<10,000 years), but also suggest an undergoing process of parallel diversification of the holobiont. The cyclic seasonal fluctuations in gut microbiota composition hint to an important plasticity of these bacterial communities in response to the host annual physiological/metabolic shifts. The importance of these microbial community dynamics in the host ecology and dietary flexibility remains to be investigated.

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Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Cited by 7 publications

References 109 publications

The influence of species identity and geographic locations on gut microbiota of small rodents

The influence of species identity and geographic locations on gut microbiota of small rodents

Isolated Grauer’s gorilla populations differ in diet and gut microbiome

Insular holobionts: persistence and seasonal plasticity of the Balearic wall lizard (Podarcis lilfordi) gut microbiota

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