Native-Alien Dichotomy in Pathogen Genomics: Host Specialization Versus Environmental Decoupling

Genome size is a key genomic trait underpinning evolutionary potential and ecological adaptation in pathogens, yet its biogeographic patterns remain poorly understood. From New Zealand data, we quantify the influence of host traits versus environmental factors on biogeographic patterns of genome size in pathogenic fungi, and test whether these predictors differ between native and alien pathogens. Host plants were the strongest predictors of genome size, with effects particularly pronounced in Basidiomycota and biotrophic fungi. Within co-origin host-pathogen pairs (native-native; alien-alien), conservative host traits were associated with smaller pathogen genomes overall, but with larger genomes in Basidiomycota. Host effects were stronger in native pathogens, while environmental filtering diverged, with climate dominating in native pathogens and terrain-related factors in alien pathogens. Native pathogens exhibited pronounced geographic genomic differentiation, whereas alien pathogens showed spatial homogenization. These results reveal a hierarchical framework that enhances predictions of disease dynamics under global environmental change.