Natural selection in bats with historical exposure to white-nose syndrome

Markéta Harazim,Zuzana Vavrušová,Natália Martínková,Jiří C Moravec,Jan Zukal,Alexandra Zahradníková,Petr Sosík,Kristína Luermann,Shannon Morgan,Ivan Horáček,Jiri Pikula,Lucie Jakešová

doi:10.1186/s40850-018-0035-4

Abstract

BackgroundHibernation allows animals to survive periods of resource scarcity by reducing their energy expenditure through decreased metabolism. However, hibernators become susceptible to psychrophilic pathogens if they cannot mount an efficient immune response to infection. While Nearctic bats infected with white-nose syndrome (WNS) suffer high mortality, related Palearctic taxa are better able to survive the disease than their Nearctic counterparts. We hypothesised that WNS exerted historical selective pressure in Palearctic bats, resulting in genomic changes that promote infection tolerance.ResultsWe investigated partial sequences of 23 genes related to water metabolism and skin structure function in nine Palearctic and Nearctic hibernating bat species and one non-hibernating species for phylogenetic signals of natural selection. Using maximum likelihood analysis, we found that eight genes were under positive selection and we successfully identified amino acid sites under selection in five encoded proteins. Branch site models revealed positive selection in three genes. Hibernating bats exhibit signals for positive selection in genes ensuring tissue regeneration, wound healing and modulation of the immune response.ConclusionOur results highlight the importance of skin barrier integrity and healing capacity in hibernating bats. The protective role of skin integrity against both pathophysiology and WNS progression, in synergy with down-regulation of the immune reaction in response to the Pseudogymnoascus destructans infection, improves host survival. Our data also suggest that hibernating bat species have evolved into tolerant hosts by reducing the negative impact of skin infection through a set of adaptations, including those at the genomic level.

Highlights

Hibernation allows animals to survive periods of resource scarcity by reducing their energy expenditure through decreased metabolism
Annotated sequences of 23 genes were retrieved from the NCBI database for species in the Vespertilionidae and Miniopteridae families, namely acad10, acp5, anxa1, aqp3, aqp4, aqp7, aqp9, bcam, ctnnb1, fads1, fgf10, guca2b, has2, hyal2, hyal3, krt8, lrp4, psen2, ptch2, pxn, sncg, tgm1, and tnfsf13 (Additional file 1)
We identified four sites under positive selection in acp5, seven sites in anxa1, one site in aqp3, one site recognised from both model comparisons and one additional site identified by comparing M7 to M8 in ptch2

Summary

Introduction

Hibernation allows animals to survive periods of resource scarcity by reducing their energy expenditure through decreased metabolism. While Nearctic bats infected with white-nose syndrome (WNS) suffer high mortality, related Palearctic taxa are better able to survive the disease than their Nearctic counterparts. We hypothesised that WNS exerted historical selective pressure in Palearctic bats, resulting in genomic changes that promote infection tolerance. Carriers of alleles that facilitate less serious disease manifestation have a higher chance of survival, while gene variants causing increased susceptibility to the infection or more severe diseases are more likely to vanish from the population gene pool. Pathogens serve as a selective force in susceptible hosts, directing changes in host population genetic diversity. White-nose syndrome (WNS), a fungal infection of hibernating bats, potentially applies strong selection pressure on bat populations in the Nearctic.

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