Social and environmental transmission spread different sets of gut microbes in wild mice
: Raulo, Aura; Bürkner, Paul-Christian; Finerty, Genevieve E.; Dale, Jarrah; Hanski, Eveliina; English, Holly M.; Lamberth, Curt; Firth, Josh A.; Coulson, Tim; Knowles, Sarah C. L.
Publisher: Springer Nature
: 2024
: Nature Ecology and Evolution
: Nature ecology & evolution
: Nat Ecol Evol
: 8
: 972
: 985
: 2397-334X
: 2397-334X
DOI: https://doi.org/10.1038/s41559-024-02381-0
: https://www.nature.com/articles/s41559-024-02381-0
: https://research.utu.fi/converis/portal/detail/Publication/393447857
Gut microbes shape many aspects of organismal biology, yet how these key bacteria transmit among hosts in natural populations remains poorly understood. Recent work in mammals has emphasized either transmission through social contacts or indirect transmission through environmental contact, but the relative importance of different routes has not been directly assessed. Here we used a novel radio-frequency identification-based tracking system to collect long-term high-resolution data on social relationships, space use and microhabitat in a wild population of mice (Apodemus sylvaticus), while regularly characterizing their gut microbiota with 16S ribosomal RNA profiling. Through probabilistic modelling of the resulting data, we identify positive and statistically distinct signals of social and environmental transmission, captured by social networks and overlap in home ranges, respectively. Strikingly, microorganisms with distinct biological attributes drove these different transmission signals. While the social network effect on microbiota was driven by anaerobic bacteria, the effect of shared space was most influenced by aerotolerant spore-forming bacteria. These findings support the prediction that social contact is important for the transfer of microorganisms with low oxygen tolerance, while those that can tolerate oxygen or form spores may be able to transmit indirectly through the environment. Overall, these results suggest social and environmental transmission routes can spread biologically distinct members of the mammalian gut microbiota.
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This work was carried out under the UK Home Office project license Animals (Scientific Procedures) Act (licence number PB0178858 held by S.C.L.K.) and supported by a grant from the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs; NC/R001103/1), a Natural Environment Research Council (NERC) fellowship (NE.L011867/1) to S.C.L.K., as well as funding from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 851550). A.R. was supported by a Clarendon Scholarship. J.A.F. acknowledges funding from the Biotechnology and Biological Sciences Research Council (BB/S009752/1), NERC (NE/S010335/1 and NE/V013483/1) and WildAI (CBR00730). We thank N. Fisher and the whole Wytham Woods team for continuous support while collecting this data. We further thank F. Mazel for feedback on the manuscript, A. Downie for feedback on the social network analysis codes, T. Potter, K. Wanelik and T. Wasserman for good discussions and valuable feedback regarding the Bayesian regression models used here and M. Quicray for help with the vegetation mapping.
