Host Ecology Shapes Gut Pathogen Evolution: An Eco-Evolutionary Trade-Off in Plateau Wildlife

The intestinal tracts of plateau wildlife function as crucial reservoirs for diverse pathogens. However, the mechanisms through which host ecology influences pathogen community assembly and their interactions remain unclear. By comparing the subterranean-living plateau zokor (Eospalax baileyi) with the aboveground plateau pika (Ochotona curzoniae) across a two-and-a-half-year study, this work provides evidence that the distribution and transmission dynamics of pathogens, virulence factor genes (VFGs), and pathogen-host interaction (PHI) genes are determined by animals' distinct niches. The results demonstrate a clear eco-evolutionary trade-off: the plateau zokor, inhabiting stable yet pathogen-enriched burrow systems, exhibited higher abundances of pathogens, VFGs, and PHI genes in its gut, and formed complex co-occurrence networks. In contrast, the plateau pika, under diverse environmental exposure, possessed higher pathogen and gene diversity but lower overall abundance, alongside simpler interaction networks indicative of opportunistic colonization. Metagenomic binning indicated a close association among VFGs, PHI genes, and mobile genetic elements (MGEs), pointing to their possible joint transfer. Additionally, animal weight and precipitation were identified as key drivers of pathogen dynamics. These findings indicate that the gut sits at the crossroads of animal and environmental health, highlighting how host-mediated pathogen evolution across distinct niches shapes the broader One Health dynamics of the plateau ecosystem.