Natural selection in bats with historical exposure to white-nose syndrome

Harazim, Markéta; Horáček, Ivan; Jakešová, Lucie; Luermann, Kristína; Moravec, Jiří; Morgan, Shannon; Pikula, Jiří; Sosík, Petr; Vavrušová, Zuzana; Zahradníková, Alexandra; Zukal, Jan; Martínková, Natália

doi:10.1186/s40850-018-0035-4

Cited by 18 publications

(17 citation statements)

References 75 publications

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“…Our results indicate that the shift towards colder hibernating temperatures, where the bats are assumed to defend their body temperature [46], might be adaptive in contaminated hibernacula. While the immune competence is reduced in hibernating bats [77], their temperature choice might represent a protective mechanism to minimize pathogen pressure ( Figure 7).…”

Section: Host Resistance-susceptibility Continuummentioning

confidence: 99%

Hibernation temperature-dependentPseudogymnoascus destructansinfection intensity in Palearctic bats

et al. 2018

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White-nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans that is devastating to Nearctic bat populations but tolerated by Palearctic bats. Temperature is a factor known to be important for fungal growth and bat choice of hibernation. Here we investigated the effect of temperature on the pathogenic fungal growth in the wild across the Palearctic. We modelled body surface temperature of bats with respect to fungal infection intensity and disease severity and were able to relate this to the mean annual surface temperature at the site. Bats that hibernated at lower temperatures had less fungal growth and fewer skin lesions on their wings. Contrary to expectation derived from laboratory P. destructans culture experiments, natural infection intensity peaked between 5 and 6°C and decreased at warmer hibernating temperature. We made predictive maps based on bat species distributions, temperature and infection intensity and disease severity data to determine not only where P. destructans will be found but also where the infection will be invasive to bats across the Palearctic. Together these data highlight the mechanistic model of the interplay between environmental and biological factors, which determine progression in a wildlife disease.

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Section: Host Resistance-susceptibility Continuummentioning

confidence: 99%

Hibernation temperature-dependentPseudogymnoascus destructansinfection intensity in Palearctic bats

et al. 2018

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“…Palearctic bat species that have co-evolved with P. destructans develop only mild clinical signs [16][17][18], while susceptibility to WNS varies among Nearctic species that were first exposed since P. destructans was introduced to eastern North America [7,19,20]. Understanding the genetic and behavioral basis for interspecific variation in susceptibility to WNS has been a critical research focus since the disease was described [7,14,17,[21][22][23][24][25][26][27]. However, our understanding of the molecular response of hibernating bats to WNS is largely limited to studies of the little brown bat [Myotis lucifugus ; 8,28,29].…”

Section: Introductionmentioning

confidence: 99%

“…Characterizing interspecific variation in the molecular responses to WNS during hibernation could identify drivers of susceptibility, tolerance, and resistance to fungal infections [8,24,28] and inform studies of other fungal pathogens. It could also improve predictions of the effects of WNS as P. destructans continues to spread [17,25,31,32].…”

Section: Introductionmentioning

confidence: 99%

“…It could also improve predictions of the effects of WNS as P. destructans continues to spread [17,25,31,32]. Specifically, the accuracy of such predictions could be improved by understanding whether the molecular response of hibernating bats to P. destructans reflects evolutionary history (i.e., is more similar among related species) or reflects a species' susceptibility, tolerance, or resistance to the pathogen [24,33]. Finally, comparing the molecular response of P. destructans to growth on different species of bat could identify virulence factors produced most consistently by the fungus, which could be targeted for treatment.…”

Section: Introductionmentioning

confidence: 99%

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Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome

et al. 2020

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Understanding how context (e.g., host species, environmental conditions) drives disease susceptibility is an essential goal of disease ecology. We hypothesized that in bat white-nose syndrome (WNS), species-specific host-pathogen interactions may partly explain varying disease outcomes among host species. We characterized bat and pathogen transcriptomes in paired samples of lesion-positive and lesion-negative wing tissue from bats infected with Pseudogymnoascus destructans in three parallel experiments. The first two experiments analyzed samples collected from the susceptible Nearctic Myotis lucifugus and the less-susceptible Nearctic Eptesicus fuscus, following experimental infection and hibernation in captivity under controlled conditions. The third experiment applied the same analyses to paired samples from infected, free-ranging Myotis myotis, a less susceptible, Palearctic species, following natural infection and hibernation (n = 8 sample pairs/species). Gene expression by P. destructans was similar among the three host species despite varying environmental conditions among the three experiments and was similar within each host species between saprophytic contexts (superficial growth on wings) and pathogenic contexts (growth in lesions on the same wings). In contrast, we observed qualitative variation in host response: M. lucifugus and M. myotis exhibited systemic responses to infection, while E. fuscus upregulated a remarkably localized response. Our results suggest potential phylogenetic determinants of response to WNS and can inform further studies of context-dependent host-pathogen interactions.

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“…Since the discovery of WNS in North America in early 2006, 13 species of bats have been diagnosed with the disease in 34 U.S. states and 7 Canadian provinces (www.whitenosesyndrome.org 2020). Genetic evidence suggests that Pseudogymnoascus destructans, the causative agent of WNS, was introduced to North America from Europe (Wibbelt et al 2010;Ren et al 2012;Lorch et al 2013;Minnis and Lindner 2013;Campana et al 2017), where affected species do not experience associated mortality (Puechmaille et al 2011;Warnecke et al 2012;Wibbelt et al 2013;Zukal et al 2016;Harazim et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Changes in Genetic Diversity in a Population of Myotis lucifugus Affected by White-Nose Syndrome

Lilley

Wilson

Field

et al. 2020

G3 Genes|Genomes|Genetics

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Novel pathogens can cause massive declines in populations, and even extirpation of hosts. But disease can also act as a selective pressure on survivors, driving the evolution of resistance or tolerance. Bat white-nose syndrome (WNS) is a rapidly spreading wildlife disease in North America. The fungus causing the disease invades skin tissues of hibernating bats, resulting in disruption of hibernation behavior, premature energy depletion, and subsequent death. We used whole-genome sequencing to investigate changes in allele frequencies within a population of Myotis lucifugus in eastern North America to search for genetic resistance to WNS. Our results show low FST values within the population across time, i.e., prior to WNS (Pre-WNS) compared to the population that has survived WNS (Post-WNS). However, when dividing the population with a geographical cut-off between the states of Pennsylvania and New York, a sharp increase in values on scaffold GL429776 is evident in the Post-WNS samples. Genes present in the diverged area are associated with thermoregulation and promotion of brown fat production. Thus, although WNS may not have subjected the entire M. lucifugus population to selective pressure, it may have selected for specific alleles in Pennsylvania through decreased gene flow within the population. However, the persistence of remnant sub-populations in the aftermath of WNS is likely due to multiple factors in bat life history.

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Natural selection in bats with historical exposure to white-nose syndrome

Cited by 18 publications

References 75 publications

Hibernation temperature-dependentPseudogymnoascus destructansinfection intensity in Palearctic bats

Hibernation temperature-dependentPseudogymnoascus destructansinfection intensity in Palearctic bats

Transcriptional host–pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome

Genome-Wide Changes in Genetic Diversity in a Population of Myotis lucifugus Affected by White-Nose Syndrome

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