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  • Lilley, Thomas M.; Wilson, Ian W.; Field, Kenneth A.; Reeder, DeeAnn M.; Vodzak, Megan E.; Turner, Gregory G.; Kurta, Allen; Blomberg, Anna S.; Hoff, Samantha; Herzog, Carl; Sewall, Brent J.; Paterson, Steve (2020)
    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 F-ST 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.
  • Lilley, Thomas Mikael; Anttila, Jani Valtteri; Ruokolainen, Lasse (2018)
    White-nose syndrome (WNS), affecting multiple North American bat species during the hibernation period, is a highly pathogenic disease caused by the psychrophilic fungus Pseudogymnoascus destructans (Pd). Because the fungal pathogen persists in the hibernation site environment independently of the hosts, previous theory on spatial disease dynamics cannot predict WNS epidemics. However, the ability to understand factors contributing to the spread of white-nose syndrome (WNS) in North America is crucial to the management of infected and susceptible bat populations as well as the conservation of threatened and endangered bat species. Utilizing recent theory on environmental opportunistic pathogens, we modelled the effect of (a) landscape clustering, (b) environmental conditions in hibernacula and (c) microbial competition on the spread of WNS. We used available, already published data to construct and parameterize our model, which takes into account the spatial distribution of hibernation sites, temperature conditions in both the outside ambient and hibernation site environment, bat population dynamics, dispersal and infection by the pathogen, which also has its host-independent dynamics with the environment. We also consider the effect of outside-host competition between the pathogen and other micro-organisms on spatial disease dynamics. Our model suggests that pathogen loads accumulate in poorly connected hibernacula at short host dispersal, which can help found the epidemic. In contrast, invasion of the landscape is most successful at long host dispersal distances, with homogenous hibernation site distribution and heterogeneous between-hibernation site temperatures. Also, increasing the mean temperature across hibernacula increases fungal growth rate, leading to higher disease prevalence and faster invasion rate. Increasing spatial heterogeneity in hibernaculum temperatures results in the formation of disease hotspots in warmer hibernacula, facilitating more effective spread of the disease in the landscape. Cold-adapted competing microbes can prevent invasion, and therefore, overwintering in cold hibernacula increases probability of host survival. Sites that were suboptimal for overwintering prior to WNS may have importance in preventing local extirpations. Although the model is tailored for WNS, due to pressing need for results that can assist in planning conservation measures, these novel results can be broadly applied to other environmentally transmitted diseases. A is available for this article.
  • Lilley, Thomas M.; Sävilammi, Tiina; Ossa, Gonzalo; Blomberg, Anna S.; Vasemägi, Anti; Yung, Veronica; Vendrami, David L. J.; Johnson, Joseph S. (2020)
    Despite its peculiar distribution, the biology of the southernmost bat species in the world, the Chilean myotis (Myotis chiloensis), has garnered little attention so far. The species has a north-south distribution of c. 2800 km, mostly on the eastern side of the Andes mountain range. Use of extended torpor occurs in the southernmost portion of the range, putting the species at risk of bat white-nose syndrome, a fungal disease responsible for massive population declines in North American bats. Here, we examined how geographic distance and topology would be reflected in the population structure of M. chiloensis along the majority of its range using a double digestion RAD-seq method. We sampled 66 individuals across the species range and discovered pronounced isolation-by-distance. Furthermore, and surprisingly, we found higher degrees of heterozygosity in the southernmost populations compared to the north. A coalescence analysis revealed that our populations may still not have reached secondary contact after the Last Glacial Maximum. As for the potential spread of pathogens, such as the fungus causing WNS, connectivity among populations was noticeably low, especially between the southern hibernatory populations in the Magallanes and Tierra del Fuego, and more northerly populations. This suggests the probability of geographic spread of the disease from the north through bat-to-bat contact to susceptible populations is low. The study presents a rare case of defined population structure in a bat species and warrants further research on the underlying factors contributing to this. See the graphical abstract here.
  • Meierhofer, Melissa; Lilley, Thomas M.; Ruokolainen, Lasse; Johnson, Joseph; Parratt, Steven; Morrison, Michael; Pearce, Brian; Evans, Jonah; Anttila, Jani (2021)
    Predicting the emergence and spread of infectious diseases is critical for the effective conservation of biodiversity. White-nose syndrome (WNS), an emerging infectious disease of bats, has resulted in high mortality in eastern North America. Because the fungal causative agent Pseudogymnoascus destructans is constrained by temperature and humidity, spread dynamics may vary by geography. Environmental conditions in the southern part of the continent are different than the northeast, where disease dynamics are typically studied, making it difficult to predict how the disease will manifest. Herein, we modelled WNS pathogen spread in Texas based on cave densities and average dispersal distances of hosts, projecting these results out to 10 years. We parameterized a predictive model of WNS epidemiology and its effects on bat populations with observed cave environmental data. Our model suggests that bat populations in northern Texas will be more affected by WNS mortality than southern Texas. As such, we recommend prioritizing the preservation of large overwintering colonies of bats in north Texas through management actions. Our model illustrates that infectious disease spread and infectious disease severity can become uncoupled over a gradient of environmental variation and highlight the importance of understanding host, pathogen and environmental conditions across a breadth of environments.