Context-dependent amphibian host population response to an invading pathogen

Amphibian chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), is an emerging infectious disease that widely threatens amphibian biodiversity. However, population-level outcomes following the introduction of the pathogen are highly context dependent and are mediated by a broad suite of biotic and abiotic variables. Here, we examine the effect of the introduction of Bd on native island populations of the IUCN red-listed amphibian species Alytes muletensis, the Mallorcan midwife toad. We show that the outcome of pathogen introduction is not only dependent on biotic factors, but is also dependent on environmental factors that vary across local scales. Our experimental infections confirm that the genotype of Bd occurring on Mallorca is hypovirulent in A. muletensis when compared against the lineage found occurring on mainland Iberia. Long-term population data show that A. muletensis populations on the island are increasing overall, but trends in highly infected populations are conflicting. We use mathematical models and field data to demonstrate that this divergence in population response to infection can be explained by local environmental differences between infected sites, whereas pathogen genetics, host genetics, and intrinsic epidemiological dynamics driven by fungal load are less likely to be the cause of these differing population trajectories. Our results illustrate the need to take into account the appropriate environmental scale and context when assessing the risk that an emerging pathogen presents to a naive population or species.