The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease

Abstract

Parasites typically have broader thermal limits than hosts, so large performance gaps between pathogens and their cold- and warm-adapted hosts should occur at relatively warm and cold temperatures, respectively. We tested this thermal mismatch hypothesis by quantifying the temperature-dependent susceptibility of cold- and warm-adapted amphibian species to the fungal pathogen Batrachochytrium dendrobatidis (Bd) using laboratory experiments and field prevalence estimates from 15 410 individuals in 598 populations. In both the laboratory and field, we found that the greatest susceptibility of cold- and warm-adapted hosts occurred at relatively warm and cool temperatures, respectively, providing support for the thermal mismatch hypothesis. Our results suggest that as climate change shifts hosts away from their optimal temperatures, the probability of increased host susceptibility to infectious disease might increase, but the effect will depend on the host species and the direction of the climate shift. Our findings help explain the tremendous variation in species responses to Bd across climates and spatial, temporal and species-level variation in disease outbreaks associated with extreme weather events that are becoming more common with climate change.

Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima

“…Thus, while some studies suggest that the importance of temperature is unequivocal, other studies suggest that temperature plays virtually no role in chytridiomycosis outbreaks (Knapp et al 2011; Korfel and Hetherington 2014). While these studies do not necessarily negate the importance of temperature, they nevertheless suggest that the effects of temperature are more nuanced than we initially appreciated (Venesky et al 2014; Cohen et al 2017). …”

“…Third, rapidly changing environments are predicted to shift fungal disease dynamics, but understanding complexities of fungal responses to temperature will be important for anticipating the disease impacts (Raffel et al 2013; Rohr et al 2013). For example, it has been suggested that mismatches in thermal tolerances of Bd and amphibian hosts could drive chytridiomycosis outbreaks (Nowakowski et al 2016; Cohen et al 2017). Therefore, a shifting climate, or an introduction of a Bd strain to a thermal environment that it was not adapted to, could dramatically affect the propensity of Bd to cause an outbreak (Nowakowski et al 2016; Cohen et al 2017).…”

“…For example, it has been suggested that mismatches in thermal tolerances of Bd and amphibian hosts could drive chytridiomycosis outbreaks (Nowakowski et al 2016; Cohen et al 2017). Therefore, a shifting climate, or an introduction of a Bd strain to a thermal environment that it was not adapted to, could dramatically affect the propensity of Bd to cause an outbreak (Nowakowski et al 2016; Cohen et al 2017). …”

Effects of latitudinal, seasonal, and daily temperature variations on chytrid fungal infections in a North American frog

“…Bsal grows best at lower temperatures, with optimal growth achieved in culture at 10°-15°C and death occurring at 25°C (Martel et al 2013). Laboratory exposure experiments have demonstrated an effect of temperature on the outcome of Bd infections in amphibian hosts (e.g., Raffel et al 2012, Sonn et al 2017, though the relationship between temperature and disease variables appears to vary among hosts with different ecologies (Cohen et al 2017) and also from what one would predict based on patterns of Bd growth in vitro (Sonn et al 2017). Field studies suggest that seasonal and latitudinal temperature variations (Kriger and Hero 2006, Sapsford et al 2013, as well as microhabitat selection with respect to temperature by amphibian hosts (Richards-Zawacki 2010, Rowley and Alford 2013), can affect the dynamics and outcome of Bd infections in nature.…”

Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease

“…These results underline the importance of accounting for the effects of local environmental drivers to predict the dynamics of an invading pathogen (Cohen et al, 2018(Cohen et al, , 2017Raffel et al, 2013). These results underline the importance of accounting for the effects of local environmental drivers to predict the dynamics of an invading pathogen (Cohen et al, 2018(Cohen et al, , 2017Raffel et al, 2013).…”