Phylosymbiosis drives the distribution of pathogen-protective bacteria in Appalachian salamanders

Abstract Phylosymbiosis is an association between host-associated microbiome and host phylogeny. This pattern can arise via evolution of host traits, habitat preferences, diets, and co-diversification of hosts and microbes. Understanding the drivers of phylosymbiosis is vital for modelling disease-microbiome interactions and manipulating microbiomes in multi-host systems. This study quantifies phylosymbiosis in Appalachian salamander skin in the context of infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd), while accounting for environmental microbiome exposure. We sampled ten salamander species representing >150M years divergence, assessed their Bd infection status, and analysed their skin and environmental microbiomes. Our results reveal a significant signal of phylosymbiosis which was primarily driven by host phylogeny, whereas the local environmental pool of microbes, climate, and geography had a far smaller impact. Host-microbe co-speciation was not evident, indicating that the effect stems from the evolution of host traits influencing microbiome assembly. Wild salamanders hosted putative Bd-inhibitory strains, and their abundance correlated with Bd infection. Five Bd-inhibitory bacteria strains were unusually cosmopolitan: occurring on most host species and habitats. These generalist strains may enhance the likelihood of probiotic manipulations colonising and persisting on hosts. Our results underscore the substantial influence of host-microbiome eco-evolutionary dynamics on environmental health and disease outcomes.