Gut microbiome plasticity explains the altitudinal distribution pattern and adaptability in a small mammal species...

Altitudinal distribution patterns of species, a central focus of ecology, predominantly focus on environmental factors and only rarely on the host's intrinsic adaptive capacity. Particularly, the role of gut microbiota has not yet been studied. Here, we used the wild South China Field Mouse (Apodemus draco), a widely distributed small mammal species, as the study subject to investigate the altitudinal distribution pattern of the species and assess how gut microbiota contributes to the formation of this pattern. A total of 219 wild samples were captured in the middle section of the Qionglai Mountains, China, and 121 adult individuals were selected for metagenomic sequencing (e.g., gut microbial diversity, network topology, composition, and functional profiles). Vegetation cover of each sampling quadrat was assessed using Normalized Difference Vegetation Index. Our results indicate that A. draco exhibited a hump-shaped altitudinal distribution, but the peak abundance of A. draco corresponds to lower vegetation cover of habitats. Gut microbial diversity, complexity, robustness, energy harvesting ability, and carbohydrate utilization capacity all peaked at the mid-altitude zone, matching the host's spatial distribution pattern. Furthermore, the gut microbiome in high-altitude A. draco populations facilitates host acclimatization in extreme high-altitude niches by enhancing energy harvesting, hypoxia tolerance, and pathogen resistance.IMPORTANCEWe propose for the first time that the gut microbiome serves as a pivotal factor in structuring the altitudinal distribution pattern of species and further reveal a gut microbiota-mediated adaptive strategy underlying mammalian high-altitude adaptation. These results demonstrate that the gut microbiome fundamentally facilitates host adaptation to ecological niches. The study provides a novel insight into the factors of species' spatial distribution from a gut microbiota perspective.