Prelude to a panzootic: Gene flow and immunogenetic variation in northern little brown myotis vulnerable to bat white-nose syndrome

Abstract

The fungus that causes bat white-nose syndrome (WNS) recently leaped from eastern North America to the Pacific Coast. The pathogen's spread is associated with the genetic population structure of a host (Myotis lucifugus). To understand the fine-scale neutral and immunogenetic variation among northern populations of M. lucifugus, we sampled 1142 individuals across the species' northern range. We used genotypes at 11 microsatellite loci to reveal the genetic structure of, and directional gene flow among, populations to predict the likely future spread of the pathogen in the northwest and to estimate effective population size (N e ). We also pyrosequenced the DRB1-like exon 2 of the class II major histocompatibility complex (MHC) in 160 individuals to explore immunogenetic selection by WNS. We identified three major neutral genetic clusters: Eastern, Montane Cordillera (and adjacent sampling areas), and Haida Gwaii, with admixture at intermediate areas and significant substructure west of the prairies. Estimates of N e were unexpectedly low (289-16 000). Haida Gwaii may provide temporary refuge from WNS, but the western mountain ranges are not barriers to its dispersal in M. lucifugus and are unlikely to slow its spread. Our major histocompatibility complex (MHC) data suggest potential selection by WNS on the MHC, but gene duplication limited the immunogenetic analyses.

Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white‐nose syndrome

“…Thus, microsatellite genotypes could not be recovered for all samples. As a result, heterozygous genotypes scored from our high‐throughput sequencing differed from the previous results obtained using traditional PCR methods (Davy et al., ) by −25% to −42%. The STR‐FM analysis, which does not rely on aligning reads to the genome, was also unable to generate genotypes for more than two microsatellite markers using a subset of our samples (data not shown).…”

“…Our assay revealed subtle immunogenetic variation and structure on a relatively small geographic scale, suggestive of local immunogenetic adaptation within an otherwise panmictic population (Figures a and a; Davy et al., ). Comparisons of samples taken before and after the arrival of WNS suggest a nonrandom removal of genetic variants in the immunome by P. destructans (Figures b and b).…”

“…For each of these three scenarios, we used the gatk to calculate the number of heterozygotes for each marker using a subset of our data that included only the 36 ON samples and the 28 MB samples. These 64 samples were previously genotyped based on traditional PCR amplification and sequencing of 11 microsatellite markers (Davy et al., ). We calculated the number of heterozygotes for each of these markers, to assess whether our sequence capture assay could be used to build on previous microsatellite‐based studies.…”

“…The MHC Drb1 locus in M. lucifugus is among the most polymorphic recorded in mammals to date (Palmer et al., ). Pyrosequencing of 160 individuals sampled across Canada suggests that balancing selection has maintained similar MHC diversity among genetically differentiated subpopulations, which may be disrupted by WNS‐mediated immunogenetic selection (Davy et al., ). However, the extreme observed polymorphism of the Drb1 locus in M. lucifugus is due partly to multiple gene duplications, which limits the use of these data.…”

Life in a northern town: rural villages in the boreal forest are islands of habitat for an endangered bat

“…The pathogen is moving westward and may cover much (if not all) of the species’ distributional range (Davy et al. ). White‐nose syndrome has not yet been detected in the vast boreal forest of northwestern North America, and it may be a high priority region for the conservation and recovery of little brown bats.…”