Captivity drives multi-generational shifts in the gut microbiome that mirror changing animal fitness

Gut microbiomes can dramatically affect host health and fitness, but can shift rapidly under changing environmental conditions. Understanding the interplay between microbiota, environmental pressures, and host responses is critical for predicting species' resilience, particularly in populations transitioning from the wild to human care for conservation breeding. Although captivity can profoundly alter microbial communities and host physiology, the dynamics of these transitions across generations remain poorly understood. We evaluated gut microbiota and fitness metrics in the endangered Pacific pocket mouse (Perognathus longimembris pacificus) during the establishment of a conservation breeding and reintroduction program, spanning five generations. Microbiome composition shifted gradually, stabilizing into a distinct captivity-associated state after two to three generations. These transitions paralleled changes in host weight and reproductive performance, suggesting coordinated host-microbiome adaptation. In addition, we identified microbial taxa correlated with successful reproduction, highlighting potential microbial markers of fitness. Our findings provide the first characterization of gut microbiota in Pacific pocket mice and demonstrate how captivity shapes host-microbiome systems across generations. More broadly, they underscore the importance of considering microbiome dynamics in conservation management and suggest that microbial responses to environmental change may require multiple generations to reach a new stable state.IMPORTANCEIn human-altered landscapes, animals face numerous threats to their survival, yet little is known about how rapid environmental change affects host-microbiome dynamics across generations. Microbial communities play critical roles in host nutrition, immunity, and overall fitness, and shifts in composition may alter an organism's ability to adapt. We examined the gut microbiota of the endangered Pacific pocket mouse during the transition from wild to captive environments and across four descendant generations. We found that the microbiome did not immediately shift with captivity but instead stabilized into a distinct, captivity-associated state only after several generations. This study provides the first characterization of gut microbiota in pocket mice and is the first to show, at this resolution, how a wildlife species' microbiome adapts to environmental change while tracking health and fitness across generations. Our findings highlight the need to incorporate microbiome dynamics into conservation breeding and management strategies.