Environmental conditions drive selection and recovery following disease-induced declines

Abstract

Emerging infectious diseases threaten public health and biodiversity across the globe1,2. Disease outcomes are frequently dependent on local environmental conditions3-5, but how these factors shape host adaptation and long-term recovery are often unknown6. Here we combine two decades of population, disease, and environmental data with a common garden experiment to investigate the drivers of variable declines and recovery for remnant bat populations following the emergence of the fungal disease, white-nose syndrome. We find that initial declines were greater and faster in warmer sites (88.3% vs. 74.2% in cold sites), but these populations recovered more quickly and hosts developed higher resistance (1.5x reduction of fungal loads) than populations from colder sites that were buffered from initial impacts. Our experimental data suggest that warm sites served as hotspots of host adaptation where selective pressures were stronger because thermal conditions approached optimal growth for the pathogen, which eventually favored the development of high pathogen resistance. Populations in colder sites experienced weaker selective pressure and thus remain more susceptible, although bats from larger colonies were more likely to survive, suggesting that adaptive traits exist in these populations, but at much lower frequency. These findings show that the environmental conditions that initially buffer populations from collapse can simultaneously constrain their evolutionary response to emerging threats, and ultimately determine differential recovery following disease-induced declines.