Viral metagenomics reveals heterogeneity in mammalian virus hosting, sharing, and spillover

Zoonotic viruses originating from mammals pose a persistent threat to global health. While rodents and bats are often considered "special reservoirs," it is debated if spillover risk is driven by specific taxa or merely reflects mammalian species richness. However, most tests have focused on published host-virus association datasets, which can reflect systematic biases in host and virus sampling effort. To address this limitation, we analyzed a comprehensive repository of 4,685 metagenomic datasets, minimizing bias toward any one viral taxon and spanning 296 species across 14 mammalian orders. We characterized the global mammalian virome and found substantial heterogeneity in the capacity of different mammalian orders to harbor and share human-associated viruses. Counter to conventional wisdom, carnivores exhibited significantly higher propensities to carry human-associated viruses, with bats ranked lower in this metric of zoonotic risk. Network analyses of viral sharing further revealed higher cross-order virus sharing among specific mammalian orders (e.g., carnivores and artiodactyls). Phylogenetic comparative analyses revealed that host life-history traits (e.g., longevity) and anthropogenic factors (e.g., urban land use) were key ecological drivers of both virus richness and transmission centrality. Our study provides a data-driven framework that challenges prevailing narratives of zoonotic risk and offers a refined strategy for prioritizing surveillance and mitigating emerging zoonotic threats.