Genome-wide changes in genetic diversity in a population ofMyotis lucifugusaffected by white-nose syndrome

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>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 <jats:italic>Myotis lucifugus</jats:italic> in eastern North America to search for genetic resistance to WNS. Our results show low F<jats:sub>ST</jats:sub> 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 <jats:italic>M. lucifugus</jats:italic> 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.</jats:p>

Ecology and impacts of white-nose syndrome on bats

“…Three studies reported evidence of genetic changes between declining and persisting M. lucifugus 136,146,147 . However, another study 148 found no such differences in M. lucifugus populations before and after WNS-induced declines but did find increased differentiation between bat populations in NY and Pennsylvania after WNS declines. Differences among these studies may be due to differences in sampling design and methodology or could reflect biological differences in selection among populations.…”

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

“…Such effective adaptive immunity may take more generations to establish in naturally evolving populations, consistent with the undetectable WNS selection on the DRB gene and presumably also other MHC genes in current bat populations. A recent study using whole‐genome sequencing data from little brown bats detected signals of WNS selection on only one immune gene, MASP1, while all the other candidate genes were involved in hibernation behavior or fat storage (Gignoux‐Wolfsohn et al., 2018), further supporting the lack of WNS selection on MHC genes and the function of alternative survival mechanisms (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.…”

Contemporary and historical selection in Tasmanian devils (Sarcophilus harrisii) support novel, polygenic response to transmissible cancer

“…At the population level, rapid evolution in response to disease can be detected by tracking changes in allele frequency before, during, and after the outbreak of disease (14,15). However, such analyses are resource-intensive and therefore still challenging in wildlife systems (but see 16,17,18). Reduced representation techniques such as restriction-site associated DNA-sequencing (RADseq) (19) have made the acquisition of genome-wide, timeseries genetic data more accessible in non-model systems (20).…”