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Resistance in persisting bat populations after white-nose syndrome invasion.

ABSTRACT: Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat (Myotis lucifugus) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans, which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting populations than in declining populations where the fungus has recently invaded. Fitted models indicate that this is most consistent with a reduction in the growth rate of the pathogen when fungal loads become high. The data are inconsistent with the evolution of tolerance or an overall reduced pathogen growth rate that might be caused by environmental factors. The existence of resistance in some persisting populations of little brown bats offers a glimmer of hope that a precipitously declining species will persist in the face of this deadly pathogen.This article is part of the themed issue 'Human influences on evolution, and the ecological and societal consequences'.

SUBMITTER: Langwig KE

PROVIDER: S-EPMC5182440 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Resistance in persisting bat populations after white-nose syndrome invasion.

Langwig Kate E KE Hoyt Joseph R JR Parise Katy L KL Frick Winifred F WF Foster Jeffrey T JT Kilpatrick A Marm AM

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20170101 1712

Increases in anthropogenic movement have led to a rise in pathogen introductions and the emergence of infectious diseases in naive host communities worldwide. We combined empirical data and mathematical models to examine changes in disease dynamics in little brown bat (Myotis lucifugus) populations following the introduction of the emerging fungal pathogen Pseudogymnoascus destructans, which causes the disease white-nose syndrome. We found that infection intensity was much lower in persisting po ...[more]

PMID: 27920389

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Project description:The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus, Eptesicus fuscus, and Perimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen, Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans was present. Key bacterial families-including those potentially involved in pathogen defense-significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence of P. destructans for any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome in M. lucifugus but not for other bat species impacted by the disease.IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes of Myotis lucifugus and Perimyotis subflavus indicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd.

Project description:White-nose syndrome (WNS) is an emerging fungal disease of bats caused by Pseudogymnoascus destructans. Since it was first detected near Albany, NY, in 2006, the fungus has spread across eastern North America, killing unprecedented numbers of hibernating bats. The devastating impacts of WNS on Nearctic bat species are attributed to the likely introduction of P. destructans from Eurasia to naive host populations in eastern North America. Since 2006, the disease has spread in a gradual wavelike pattern consistent with introduction of the pathogen at a single location. Here, we describe the first detection of P. destructans in western North America in a little brown bat (Myotis lucifugus) from near Seattle, WA, far from the previously recognized geographic distribution of the fungus. Whole-genome sequencing and phylogenetic analyses indicated that the isolate of P. destructans from Washington grouped with other isolates of a presumed clonal lineage from the eastern United States. Thus, the occurrence of P. destructans in Washington does not likely represent a novel introduction of the fungus from Eurasia, and the lack of intensive surveillance in the western United States makes it difficult to interpret whether the occurrence of P. destructans in the Pacific Northwest is disjunct from that in eastern North America. Although there is uncertainty surrounding the impacts of WNS in the Pacific Northwest, the presence of the pathogen in western North America could have major consequences for bat conservation. IMPORTANCE White-nose syndrome (WNS) represents one of the most consequential wildlife diseases of modern times. Since it was first documented in New York in 2006, the disease has killed millions of bats and threatens several formerly abundant species with extirpation or extinction. The spread of WNS in eastern North America has been relatively gradual, inducing optimism that disease mitigation strategies could be established in time to conserve bats susceptible to WNS in western North America. The recent detection of the fungus that causes WNS in the Pacific Northwest, far from its previous known distribution, increases the urgency for understanding the long-term impacts of this disease and for developing strategies to conserve imperiled bat species.

Project description:Across the entire distribution of a species, populations may have variable responses to environmental perturbations. Many bat species experience mortality in large portions of their range during hibernation and along migratory paths to and from wintering grounds, from White-nose syndrome (WNS) and wind energy development, respectively. In some areas, warm temperatures may allow bats to remain active through winter, thus decreasing their susceptibility to WNS and/or mortality associated with migration to wintering grounds. These areas could act as a refugia and be important for the persistence of local populations. To determine if warmer temperatures affect bat activity, we compared year-round activity of bat populations in the Coastal Plain and Piedmont of North Carolina, USA, two regions that differ in winter temperature. We established six recording stations, four along a 295-kilometer north-south transect in the Coastal Plain, and two in the Piedmont of North Carolina. We recorded bat activity over two years. We supplemented our recordings with mist-net data. Although bat activity was lower during winter at all sites, the odds of recording a bat during winter were higher at Coastal Plain sites when compared with Piedmont sites. Further, bats in the Piedmont had a lower level of winter activity compared to summer activity than bats in the Coastal Plain that had more similar levels of activity in the winter and summer. We found high bat species richness on the Coastal Plain in winter, with winter-active species including those known to hibernate throughout most of their range and others known to be long distance migrants. In particular, two species impacted by WNS, the northern long-eared bat (Myotis septentrionalis) and tricolored bat (Perimyotis subflavus), were present year round in the Coastal Plain. The tricolored bat was also present year-round in the Piedmont. In the Coastal Plain, the long distance migratory hoary bat (Lasiurus cinereus) was active in the winter but not present during the other seasons, and the long distance migratory silver-haired bat (Lasionycteris noctivagans) was active primarily in the winter, suggesting the Coastal Plain may be an overwintering ground for these two species. We suggest that the winter activity exhibited by populations of bats on the North Carolina Coastal Plain has important conservation implications and these populations should be carefully monitored and afforded protection.

Project description:BackgroundInfectious diseases of wildlife are increasing worldwide with implications for conservation and human public health. The microbiota (i.e. microbial community living on or in a host) could influence wildlife disease resistance or tolerance. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans (Pd), has killed millions of hibernating North American bats since 2007. We characterized the skin microbiota of naïve, pre-WNS little brown bats (Myotis lucifugus) from three WNS-negative hibernation sites and persisting, previously exposed bats from three WNS-positive sites to test the hypothesis that the skin microbiota of bats shifts following WNS invasion.ResultsUsing high-throughput 16S rRNA gene sequencing on 66 bats and 11 environmental samples, we found that hibernation site strongly influenced the composition and diversity of the skin microbiota. Bats from WNS-positive and WNS-negative sites differed in alpha and beta diversity, as well as in microbiota composition. Alpha diversity was reduced in persisting, WNS-positive bats, and the microbiota profile was enriched with particular taxa such Janthinobacterium, Micrococcaceae, Pseudomonas, Ralstonia, and Rhodococcus. Some of these taxa are recognized for their antifungal activity, and specific strains of Rhodococcus and Pseudomonas are known to inhibit Pd growth. Composition of the microbial community in the hibernaculum environment and the community on bat skin was superficially similar but differed in relative abundance of some bacterial taxa.ConclusionsOur results are consistent with the hypothesis that Pd invasion leads to a shift in the skin microbiota of surviving bats and suggest the possibility that the microbiota plays a protective role for bats facing WNS. The detection of what appears to be enrichment of beneficial bacteria in the skin microbiota of persisting bats is a promising discovery for species re-establishment. Our findings highlight not only the potential value of management actions that might encourage transmission, growth, and establishment of beneficial bacteria on bats, and within hibernacula, but also the potential risks of such management actions.

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Resistance in persisting bat populations after white-nose syndrome invasion.

Publications

Resistance in persisting bat populations after white-nose syndrome invasion.

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