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

Abstract

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.

Major histocompatibility complex variation is similar in little brown bats before and after white‐nose syndrome outbreak

“…Similarly, a study found that a frog population maintained susceptible to chytridiomycosis despite the generation of Bd-specific antibodies, suggesting ineffective adaptive immune responses to the fungal disease (Ellison et al, 2014). For hibernating bats, initiation of normally suppressed immune responses would interrupt torpor and deplete energy storage (Bouma et al, 2010;Field et al, 2015Field et al, , 2018Lilley et al, 2017;Moore et al, 2013;Rapin et al, 2014), both increasing the chance of mortality (Reeder et al, 2012;Verant et al, 2014;Warnecke et al, 2012 (Lilley et al, 2020).…”

“…For highly variable loci like the MHC gene, bottlenecks might have little impact on heterozygosity, but genetic drift during the decline of population size can cause substantial losses of rare alleles and allelic richness (Eimes et al, 2011;Sutton et al, 2015). In fact, demographic bottlenecks were observed in PA sites during sampling given the high rate of WNS-related mortality and rarity of surviving bats (but see Lilley et al, 2020). Individuals from VT were proposed to have similar MHC allelic diversity as the nearby NY individuals based on high levels of regional gene flow (Vonhof et al, 2015); however, our data showed relatively lower allelic richness and a weak genetic distinction of the VT samples, similar to the lowest post-WNS allele frequencies among VT individuals detected in another study (Gignoux-Wolfsohn et al, 2018).…”

“…According to the results in this study, we suggest that resistance through adaptive immunity is not the current mechanism of persistence in little brown bat populations affected by WNS. Other resistance or tolerance mechanisms related to physiological and behavioral changes may be more effective to increase present survival (Auteri & Knowles, 2020;Johnson et al, 2015;Lilley et al, 2020), such as through skin microbiome (Ange-Stark et al, 2019;Hoyt et al, 2019), increased fat storage (Cheng et al, 2019), and altered hibernating behavior (Gignoux-Wolfsohn et al, 2018;Reeder et al, 2012). These physiological and behavioral mechanisms may also help to give time for effective adaptive immunity to evolve in natural populations.…”

Genomic signatures of selection in bats surviving white‐nose syndrome

“…REPS2 is a part of the Ras/Ral signalling pathway, which is important for receptor-mediated endocytosis (Badway & Baleja, 2011). None of the genes identified by previous studies of WNS-induced selection (Auteri & Knowles, 2020;Donaldson et al, 2017;Lilley et al, 2020) were differentially expressed between infected and uninfected bats. Taken together, our study and Field et al (2018) provide strong evidence that PCDH17 and REPS2 may be involved in the host response to Pseudogymnoascus destructans and should be further investigated as genes associated with resistance.…”

“…A recent study identified signatures of selection in M. lucifugus by comparing WNS survivors and nonsurvivors from across Michigan, USA, where populations are continuing to decline, suggesting that WNS can select for alleles related to hibernation behaviour, metabolism and vocalization (Auteri & Knowles, 2020). Despite the hypothesis that immune-related genes are probable targets of WNS-related selection (Donaldson et al, 2017), immune-related genes were not apparent targets of selection in Michigan (Auteri & Knowles, 2020), a result compatible with survivor allele frequency differences between New York and Pennsylvania (Lilley et al, 2020). Whether targets of selection are consistent across different geographical regions remains unclear, however.…”