Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome

Department of Biology and Centre for Forest Interdisciplinary Research, University of Winnipeg, Winnipeg, MB, Canada R3B 2E9.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 04/2012; 109(18):6999-7003. DOI: 10.1073/pnas.1200374109
Source: PubMed


White-nose syndrome (WNS) is an emerging disease of hibernating bats associated with cutaneous infection by the fungus Geomyces destructans (Gd), and responsible for devastating declines of bat populations in eastern North America. Affected bats appear emaciated and one hypothesis is that they spend too much time out of torpor during hibernation, depleting vital fat reserves required to survive the winter. The fungus has also been found at low levels on bats throughout Europe but without mass mortality. This finding suggests that Gd is either native to both continents but has been rendered more pathogenic in North America by mutation or environmental change, or that it recently arrived in North America as an invader from Europe. Thus, a causal link between Gd and mortality has not been established and the reason for its high pathogenicity in North America is unknown. Here we show that experimental inoculation with either North American or European isolates of Gd causes WNS and mortality in the North American bat, Myotis lucifugus. In contrast to control bats, individuals inoculated with either isolate of Gd developed cutaneous infections diagnostic of WNS, exhibited a progressive increase in the frequency of arousals from torpor during hibernation, and were emaciated after 3-4 mo. Our results demonstrate that altered torpor-arousal cycles underlie mortality from WNS and provide direct evidence that Gd is a novel pathogen to North America from Europe.

Download full-text


Available from: Gudrun Wibbelt,
  • Source
    • "Our results strongly suggest that active management is required to increase little brown bat recovery potential. Despite several advances in understanding the ecology of P. destructans and its effects on bats (e.g., Warnecke et al. 2012, Langwig et al. 2015), a clear path toward effective management of this pathogen is not yet apparent. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Management of wildlife populations impacted by novel threats is often challenged by a lack of data on temporal changes in demographic response. Populations may suffer rapid declines from the introduction of new stressors, but how demography changes over time is critical to determining long-term outcomes for populations. White-nose syndrome (WNS), an infectious disease of hibernating bats, has caused massive and rapid population declines in several hibernating species of bats in North America since the disease was first observed on the continent in 2006. Estimating annual survival rates and demographic trends among remnant colonies of hibernating bats that experienced mass mortality from WNS is needed to determine long-term population viability of species impacted by this disease. Using mark–recapture data on infected little brown bats (Myotis lucifugus), we estimated the first apparent annual survival rates for four years following WNS detection at a site. We found strong support for an increasing trend in annual survival, which improved from 0.68 (95% CI ¼ 0.44–0.85) to 0.75 (95% CI ¼ 0.51–0.89) for males and 0.65 (95% CI ¼ 0.44– 0.81) to 0.70 (95% CI ¼ 0.50–0.84) for females. These results suggest that stabilization at remnant colonies after mass mortality from WNS may be due to improved survival and not from immigration from other areas. Despite ameliorating survival, our stochastic matrix projection model predicts continued declines for little brown bat populations (k ¼ 0.95), raising concern for the regional persistence of this species. We conducted a vital rate sensitivity analysis and determined that adult and juvenile survival, as opposed to fecundity, are the demographic parameters most important to target to maximize recovery potential of little brown bat populations in areas impacted by WNS.
    Ecological Applications 10/2015; 25(7):1832-1840. DOI:10.1890/14-2472.1 · 4.09 Impact Factor
  • Source
    • "such as the mildew pathogen Plasmopara viticola in Europe; Fontaine et al., 2013; or Plasmodium falciparum, the pathogen that causes Malaria in South America; Yalcindag et al., 2012). However, there are still few case studies using the full potential of ABC to unravel the spatio-temporal dynamics of wildlife emerging pathogens (or even non-native free-living species) for which spatial and/or temporal data (from the native or non-native areas) are scarce, a characteristic of most datasets concerning emerging pathogens (e.g. for Pseudogymnoascus destructans -the species causing the white-nose disease-when it was first discovered; Warnecke et al., 2010). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Emerging pathogens constitute a severe threat for human health and biodiversity. Determining the status (native or non-native) of emerging pathogens, and tracing back their spatio-temporal dynamics is crucial to understand the eco-evolutionary factors promoting their emergence, to control their spread and mitigate their impacts. However, tracing back the spatio-temporal dynamics of emerging wildlife pathogens is challenging because (i) they are often neglected until they become sufficiently abundant and pose socio-economical concerns and (ii) their geographic range is often little known. Here we combined classical population genetics tools and approximate Bayesian computation (i.e. ABC) to retrace the dynamics of Tracheliastes polycolpus, a poorly documented pathogenic ectoparasite emerging in Western Europe that threatens several freshwater fish species. Our results strongly suggest that populations of T. polycolpus in France emerged from individuals originating from a unique genetic pool that were most likely introduced in the 1920's in central France. From this initial population, three waves of colonization occurred into peripheral watersheds within the next two decades. We further demonstrated that populations remained at low densities, and hence undetectable, during ten years before a major demographic expansion occurred, and before its official detection in France. These findings corroborate and expand the few historical records available for this emerging pathogen. More generally, our study demonstrates how ABC can be used to determine the status, reconstruct the colonization history, and infer key evolutionary parameters of emerging wildlife pathogens with low data availability, and for which samples from the putative native area are inaccessible. This article is protected by copyright. All rights reserved.
    Molecular Ecology 09/2015; 24(21):5348-5363. DOI:10.1111/mec.13401 · 6.49 Impact Factor
  • Source
    • "A particularly virulent fungal pathogen (Pseudogymnoascus destructans; Pd) emerged in hibernating bats in eastern North America in 2006 (Blehert et al. 2009; Minnis and Lindner 2013). Likely an introduced species to North America (Warnecke et al. 2012), Pd has spread rapidly since its discovery. In the laboratory, infection is spread by physical contact between bats (i.e. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Viral, bacterial, parasitic and fungal pathogens pose a significant, current threat to global biodiversity. A virulent fungal pathogen (Pseudogymnoascus destructans; Pd) emerged in hibernating bats in eastern North America in 2006. In this paper, we seek to inform epidemiological models of the progression of Pd into populations of the little brown bat (Myotis lucifugus) in central Canada by characterizing the spatial genetic structure of the host ahead of the imminent arrival of Pd. We sampled 242 bats from eight hibernacula spanning 92,623 km 2 and two ecozones. We genotyped all individuals at eight mi-crosatellite loci and sequenced 300 bp of HVII in a subset (n = 72) to test the null hypothesis of contemporary pan-mixia. We found evidence of spatial genetic structure associated with ecozone boundaries, and a predominant north–west to south–east directionality of bat movements among hibernacula, which opposes the current approach of the pathogen. Our large study area (larger than the dispersal distance of individual bats) allowed us to detect the first evidence of contemporary population structure among hibernacula of M. lucifugus. Our results suggest that the potential spread of Pd into north-central Canada may be retarded by the opposing direction of gene flow of the host species, and our findings of directional gene flow can be used to inform management strategies for the spread of Pd into the area. Keywords White nose syndrome Á Little brown bat Á Central North America Á Spatial genetic structure Á Hibernacula Á Ecozones
    Conservation Genetics 04/2015; 16(5). DOI:10.1007/s10592-015-0719-z · 2.19 Impact Factor
Show more