Abstract
Mitigation of emerging infectious diseases that threaten global biodiversity requires an understanding of critical host and pathogen responses to infection. For multihost pathogens where pathogen virulence or host susceptibility is variable, host–pathogen interactions in tolerant species may identify potential avenues for adaptive evolution in recently exposed, susceptible hosts. For example, the fungus Pseudogymnoascus destructans causes white‐nose syndrome (WNS) in hibernating bats and is responsible for catastrophic declines in some species in North America, where it was recently introduced. Bats in Europe and Asia, where the pathogen is endemic, are only mildly affected. Different environmental conditions among Nearctic and Palearctic hibernacula have been proposed as an explanation for variable disease outcomes, but this hypothesis has not been experimentally tested. We report the first controlled, experimental investigation of response to P. destructans in a tolerant, European species of bat (the greater mouse‐eared bat, Myotis myotis). We compared body condition, disease outcomes and gene expression in control (sham‐exposed) and exposed M. myotis that hibernated under controlled environmental conditions following treatment. Tolerant M. myotis experienced extremely limited fungal growth and did not exhibit symptoms of WNS. However, we detected no differential expression of genes associated with immune response in exposed bats, indicating that immune response does not drive tolerance of P. destructans in late hibernation. Variable responses to P. destructans among bat species cannot be attributed solely to environmental or ecological factors. Instead, our results implicate coevolution with the pathogen, and highlight the dynamic nature of the “white‐nose syndrome transcriptome.” Interspecific variation in response to exposure by the host (and possibly pathogen) emphasizes the importance of context in studies of the bat‐WNS system, and robust characterization of genetic responses to exposure in various hosts and the pathogen should precede any attempts to use particular bat species as generalizable “model hosts.”
Highlights
The impacts of pathogenic fungi on vertebrate hosts range widely, from mild symptoms in some circumstances, to rapid extinction in others (Ellison et al, 2015; Fisher et al, 2012; Hoyt et al, 2015; Langwig et al, 2015; Perez-Nadales et al, 2014)
The application of our methods to susceptible M. lucifugus hibernating under the same environmental conditions resulted in high fungal loads from which P. destructans RNA could be isolated and sequenced, and caused clinical white-nose syndrome (WNS) characterized by lethargic behavior and substantial, obvious fungal lesions on the wings that fluoresced under UV light (Warnecke et al, 2012; Supporting information)
Exposure to high doses of P. destructans did not cause M. myotis to develop symptoms of WNS, despite hibernating under controlled environmental conditions that mimicked those selected by wild, susceptible M. lucifugus
Summary
The impacts of pathogenic fungi on vertebrate hosts range widely, from mild symptoms in some circumstances, to rapid extinction in others (Ellison et al, 2015; Fisher et al, 2012; Hoyt et al, 2015; Langwig et al, 2015; Perez-Nadales et al, 2014). Characterizing the response of tolerant or resistant vertebrate hosts to fungal infections can identify adaptive genes or processes linked to reduced disease severity or occurrence (Ellison et al, 2015; Rosenblum et al, 2012) These can inform studies of susceptible species, including species recently exposed to the pathogen, where insufficient time has elapsed for selection for tolerance to occur. In contrast to the North American situation, European and Asian bats exhibit mild symptoms or remain asymptomatic following exposure to P. destructans, and no WNS-related mass mortality has been documented on either continent (Hoyt et al, 2016a,b; Wibbelt et al, 2010; Zukal et al, 2016) These outcomes may reflect tolerance (the host experiences pathogen loads comparable to those of susceptible species, but does not exhibit severe disease symptoms), or resistance (the host exhibits significantly lower pathogen loads compared to susceptible species). We attempted to apply a dual RNA-seq approach to explore the response of P. destructans to a tolerant host
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