Data from: Small-scale spatial variation in infection risk shapes the evolution of a Borrelia resistance gene in wild rodents

Spatial variation in pathogen-mediated selection is predicted to influence the evolutionary trajectory of host populations and lead to spatial variation in their immunogenetic composition. However, to date few studies have been able to directly link small-scale spatial variation in infection risk to host immune gene evolution in natural, non-human populations. Here we use a natural rodent-Borrelia system to test for associations between landscape-level spatial variation in Borrelia infection risk along replicated elevational gradients in the Swiss Alps and Toll-like receptor 2 (TLR2) evolution, a candidate gene for Borrelia resistance, across bank vole (Myodes glareolus) populations. We found that Borrelia infection risk (i.e. the product of Borrelia prevalence in questing ticks and the average tick load of voles at a sampling site) was spatially variable and significantly negatively associated with elevation. Across sampling sites, Borrelia prevalence in bank voles was significantly positively associated with Borrelia infection risk along the elevational clines. We observed a significant association between naturally occurring TLR2 polymorphisms in hosts and their Borrelia infection status. The TLR2 variant associated with a reduced likelihood of Borrelia infection was most common in rodent populations at lower elevations that face a high Borrelia infection risk, and its frequency changed in accordance with the change in Borrelia infection risk along the elevational clines. These results suggest that small-scale spatial variation in parasite-mediated selection affects the immunogenetic composition of natural host populations, providing a striking example that the microbial environment shapes the evolution of the host’s immune system in the wild.

病原体介导选择的空间变异，被认为会影响宿主种群的演化轨迹，并驱动其免疫遗传组成产生空间分化。但迄今鲜有研究能够在自然非人宿主种群中，直接将感染风险的小规模空间变异与宿主免疫基因演化建立关联。本研究依托自然啮齿类-疏螺旋体（Borrelia）宿主系统，在瑞士阿尔卑斯山的重复海拔梯度上，检验疏螺旋体感染风险的景观级空间变异，与棕背䶄（Myodes glareolus）种群中作为疏螺旋体抗性候选基因的Toll样受体2（TLR2）演化之间的关联。研究发现，疏螺旋体感染风险（即游离蜱的疏螺旋体感染率与采样位点内棕背䶄平均蜱负荷的乘积）存在空间异质性，且与海拔呈显著负相关。在所有采样位点中，棕背䶄体内的疏螺旋体感染率与海拔梯度上的疏螺旋体感染风险呈显著正相关。我们观测到宿主天然存在的TLR2多态性与其疏螺旋体感染状态之间存在显著关联。与降低疏螺旋体感染概率相关的TLR2变异体，在面临高感染风险的低海拔啮齿类种群中分布最为广泛，且其频率随海拔梯度上的疏螺旋体感染风险变化而发生对应改变。上述结果表明，寄生虫介导选择的小规模空间变异会影响自然宿主种群的免疫遗传组成，为野外环境中微生物环境塑造宿主免疫系统演化提供了极具说服力的例证。