Conserved patterns of mammal-microbe codiversification and interspecific bacterial sharing

What determines whether a gut microbial lineage has fidelity to one host species or is shared freely across multiple species? Factors that predict microbial community composition, including host species, diet, and environmental variation, have been well documented in wild animals. However, the eco-evolutionary processes maintaining host species- or population-specific microbial lineages remain unresolved. Here, we analyze 519 gut microbiome samples collected from 15 species of wild rodents across two mountains in the Madrean Sky Islands of southeastern Arizona using full-length 16S rRNA sequencing. This montane system provides a natural experiment in which adjacent replicated elevational gradients bring different combinations of rodent species into sympatry, allowing host evolutionary history to be disentangled from shared environmental effects. We find that host phylogeny, rather than environment, is the primary driver of microbial strain sharing across host species. We recover replicated signatures of codiversification on both mountains, indicating shared evolutionary history between hosts and their microbes, despite ample opportunities for cross-species environmental transmission. This evolutionary coupling is associated with predicted differences in bacterial oxygen tolerance and optimal growth temperature: codiversifying lineages are predominantly obligate anaerobes with optimal growth near host body temperature, suggesting more limited out-of-host persistence than non-codiversifying taxa. This pattern mirrors findings from the human gut microbiome, suggesting conserved constraints on microbial dispersal across mammalian hosts. The cost-effectiveness of long-read amplicon sequencing for phylogenetic inference within bacterial species opens new opportunities for large-scale evolutionary and ecological studies of host-microbe interactions in wildlife.