Wild wood mouse gut microbiota are influenced by captivity and cross-fostering

Background Wild and laboratory animals harbour profoundly different gut microbiota, but how microbiomes shift between these states, and the relative roles of captivity, microbial history, and host identity in shaping that shift, remain unclear. Here, we developed a unique wood mouse (Apodemus sylvaticus) system comprising free-living mice (Wild:As), a wild-derived colony maintained in captivity for over a decade (Wild-like:As), and a second colony that we generated from the Wild-like:As mice by caesarean rederivation and cross-fostering to laboratory Mus musculus (Lab-like:As). We compared these three Apodemus cohorts with conventional laboratory Mus musculus (Lab:Mm) to ask how microbial diversity, community composition, and functional potential vary across a spectrum of wild-to-laboratory conditions. Results We found that alpha diversity varied substantially among cohorts but showed no consistent wild-to-laboratory trend: Shannon diversity was higher in Lab:Mm and Lab-like:As than in Wild:As and Wild-like:As mice, whereas phylogenetic diversity was similarly high in both the Wild:As and Lab:Mm groups. Community composition more closely reflected cohort histories. Despite over a decade in captivity, Wild-like:As mice remained most similar to Wild:As conspecifics, whereas Lab-like:As mice shifted strongly away from Wild-like:As and toward, but remained distinct from, Lab:Mm mice. The clearest wild-to-laboratory pattern emerged in microbiome consistency: core ASVs (present in [≥]90% of individuals) increased from 9 in Wild:As to 46 in Wild-like:As, 72 in Lab-like:As, and 138 in Lab:Mm mice. Predicted functional potential revealed a further distinction between taxonomic and functional patterns: Wild:As and Wild-like:As microbiomes did not differ significantly, whereas Lab-like:As shifted toward the Lab:Mm state despite remaining taxonomically distinct. Conclusions Together, these results show that laboratory-associated microbiomes do not emerge through simple loss of wild microbial diversity, but through broader reorganisation of community composition, consistency, and predicted functional potential reflecting microbial history and host context. The persistent Wild-like and Lab-like microbiome states within Apodemus provide a powerful experimental system for future timely work testing how microbiome history influences host physiology, resilience, and responses to environmental challenges.