High phenotypic diversity correlated with genomic variation across the European Batrachochytrium salamandrivorans epizootic

Recognizing the influence of pathogen diversity on infection dynamics is crucial for mitigating emerging infectious diseases. Characterising such diversity is often complex, for instance when multiple pathogen variants exist that interact differently with the environment and host. Here, we explore genotypic and phenotypic variation of Batrachochytrium salamandrivorans (Bsal), an emerging fungal pathogen that is driving declines among an increasing number of European amphibian species. For thirteen isolates, spanning most of the known temporal and geographical Bsal range in Europe, we mapped phenotypic diversity through numerous measurements that describe varying reproductive rates in vitro across a range of temperatures. Bsal isolates are revealed to have different thermal optima and tolerances, with phenotypic variation correlating with genomic diversity. Using a mechanistic niche model of the fire salamander (Salamandra salamandra) as an example, we illustrate how host steady-state body temperature and Bsal thermal range variation may influence pathogen growth through space and time across Europe. Our combined findings show how the identity of emergent pathogen variants may strongly influence when and which host populations are most at risk.Author summary: In 2013, a new, salamander-killing fungus, Batrachochytrium salamandrivorans (Bsal) was discovered in the Netherlands. Since then, Bsal outbreaks have occurred in a growing number of countries and amphibian species across Europe, causing rapid population collapses. A lot remains unknown about this pathogen, with most studies so far focusing on the type strain from the first outbreak site. Here we show that strains from other outbreaks behave differently and may threaten different amphibian populations at different times. We found that observed phenotypic variation correlated with genotypic variation and identified molecular functions and biological processes under selection across the European Bsal epidemic. As both the fungus and the amphibian hosts are very temperature sensitive, we tested Bsal growth across a range of temperatures. We found strains displayed different thermal ranges and optimal temperatures and combined these thermal growth curves with models of amphibian host body temperatures to predict strain geographical and temporal ranges. Our findings help to explain observed Bsal epidemiology and provide insights into how strain identity strongly influences when and which host populations are most at risk, with important implications for Bsal research and amphibian conservation efforts.