Host persistence or extinction from emerging infectious disease: insights from white-nose syndrome in endemic and invading regions

Abstract

Predicting species' fates following the introduction of a novel pathogen is a significant and growing problem in conservation. Comparing disease dynamics between introduced and endemic regions can offer insight into which naive hosts will persist or go extinct, with disease acting as a filter on host communities. We examined four hypothesized mechanisms for host–pathogen persistence by comparing host infection patterns and environmental reservoirs for Pseudogymnoascus destructans (the causative agent of white-nose syndrome) in Asia, an endemic region, and North America, where the pathogen has recently invaded. Although colony sizes of bats and hibernacula temperatures were very similar, both infection prevalence and fungal loads were much lower on bats and in the environment in Asia than North America. These results indicate that transmission intensity and pathogen growth are lower in Asia, likely due to higher host resistance to pathogen growth in this endemic region, and not due to host tolerance, lower transmission due to smaller populations, or lower environmentally driven pathogen growth rate. Disease filtering also appears to be favouring initially resistant species in North America. More broadly, determining the mechanisms allowing species persistence in endemic regions can help identify species at greater risk of extinction in introduced regions, and determine the consequences for disease dynamics and host–pathogen coevolution.

The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

“…Thus, extremely low detection of P. destructans on exposed, tolerant hosts, and the absence of conidia or cupping erosions detected during histopathological examination implies potential inhibition of pathogen activity. Tolerant hosts may not need to mount an immune response if they are able to repress P. destructans growth and pathogenicity, which could potentially be accomplished through secreted skin proteins or through the secretions of commensal bacteria (Hoyt et al., 2015, 2016a,b). We note that our results suggest potential mechanisms of resistance as well as tolerance, because we did not observe pathogen loads on M. myotis comparable to those seen on M. lucifugus exposed following the same protocol (Supporting information).…”

“…Wild M. myotis do often develop mild symptoms of WNS, although disease prevalence may vary among regions (Hoyt et al., 2016a,b; Wibbelt et al., 2010; Zukal et al., 2016). It is not yet clear what drives this variation.…”

“…Interspecific variation in the initial response of bats to P. destructans could be directly tested by sampling resistant and susceptible bats shortly after exposure, prior to the development of clinical WNS. Such comparisons would ideally include North American species such as Eptesicus fuscus or Corynorhinos townsendii virginianus that may be more tolerant or resistant to infection with P. destructans (Frank et al., 2014; Hoyt et al., 2016a,b). …”

“…Comparative transcriptomics can disentangle environmental effects on disease outcomes (e.g., Hoyt et al., 2016a,b; Langwig et al., 2012) from effects mediated by context‐specific host and pathogen responses to infection (Brown et al., 2003; Poorten & Rosenblum, 2016). Appreciating the importance of context and evolutionary history in host–pathogen interactions is critical to our ability to mitigate impacts of emerging infectious diseases on biodiversity, human health, agricultural systems, and ecosystem services (Enguita et al., 2016; Jones et al., [Link]; Smith, Sax, & Lafferty, 2006).…”

“…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).…”