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Nov 21

Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.) – pnas.org

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Significance

Understanding the factors that sculpt gut microbial communities in mammals is of great interest. Here, we studied a diverse clade of herbivorous rodents (woodrats, Neotoma) with variable but well-characterized diets and habitats to quantify the relative contributions of host genetics, geography, and diet, alongside neutral processes, in structuring the gut microbiome under natural and controlled conditions. While diet and geography made significant contributions to microbiome structure, host phylogeny explained the greatest proportion of observed variation. Provision of a common diet in captivity altered natural microbial communities, with communities from different species varying in their resistance to this perturbation. Captivity increased the amount of variation explained by host phylogeny, further emphasizing the extent to which host genetics structure mammalian microbiomes.

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained 50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

Author contributions: S.B.W., C.D., K.D.K., and M.D.D. designed research; S.B.W., R.M.-M., T.E.S., D.M.K., and T.J.O. performed research; R.G. contributed new reagents/analytic tools; S.B.W., D.M.K., and R.G. analyzed data; and S.B.W., C.D., K.D.K., and M.D.D. wrote the paper.

The authors declare no competing interest.

This article is a PNAS Direct Submission.

See online for related content such as Commentaries.

This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2108787118/-/DCSupplemental.

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Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.) - pnas.org

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