Hibernation 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. We 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. Our 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.

中文翻译：

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历史上曾接触过白鼻综合症的蝙蝠的自然选择

冬眠使动物能够通过减少新陈代谢来减少能量消耗，从而在资源短缺的时期中度过。但是，如果冬眠者无法对感染进行有效的免疫反应，他们就容易受到嗜冷性病原体的感染。尽管感染了白鼻综合症（WNS）的Nearctic蝙蝠的死亡率很高，但相关的古北类群比它们的Nearctic蝙蝠更能生存。我们假设WNS在古蝙蝠上施加了历史选择性压力，导致基因组变化促进了感染的耐受性。我们调查了23个与水代谢和皮肤结构功能有关的基因的部分序列，这些基因分别来自9个古北和北非冬眠蝙蝠物种和1个非冬眠物种的自然选择系统发育信号。使用最大似然分析，我们发现八个基因处于正选择状态，并且我们成功地识别了五个编码蛋白中处于选择状态的氨基酸位点。分支位点模型揭示了三个基因中的阳性选择。冬眠蝙蝠显示出可在基因中进行阳性选择的信号，从而确保组织再生，伤口愈合和免疫应答的调节。我们的结果突出了冬眠蝙蝠中皮肤屏障完整性和愈合能力的重要性。皮肤完整性针对病理生理学和WNS进程的保护作用，与对Pseudogymnoascus destructans感染的免疫反应下调的协同作用，提高了宿主的存活率。