Spatiotemporal analyses reveal infectious disease-driven selection in a free-ranging ungulate

Infectious diseases play an important role in wildlife population dynamics by altering individual fitness, but detecting disease-driven natural selection in free-ranging populations is difficult due to complex disease-host relationships. Chronic wasting disease (CWD) is a fatal infectious prion disease in cervids for which mutations in a single gene have been mechanistically linked to disease outcomes, providing a rare opportunity to study disease-driven selection in wildlife. In Wyoming, USA, CWD has gradually spread across mule deer (Odocoileus hemionus) populations, producing natural variation in disease history to evaluate selection pressure. We used spatial variation and a novel temporal comparison to investigate the relationship between CWD and a mutation at codon 225 of the mule deer prion protein gene that slows disease progression. We found that individuals with the "slow" 225F allele were less likely to test positive for CWD, and the 225F allele was more common in herds exposed to CWD longer. We also found that in the past two decades, the 225F allele frequency increased more in herds with higher CWD prevalence. This study expanded on previous research by analyzing spatiotemporal patterns of individual- and herd-based disease data to present multiple lines of evidence for disease-driven selection in free-ranging wildlife.

传染病通过改变个体适合度，在野生动物种群动态中发挥关键作用；但由于疾病与宿主间的关系错综复杂，在自由活动的野生种群中检测疾病驱动的自然选择颇具挑战。慢性消耗病（Chronic Wasting Disease, CWD）是鹿科动物的致命传染性朊病毒疾病，单个基因的突变已在机制上与疾病转归建立关联，这为研究野生动物中的疾病驱动选择提供了难得的契机。在美国怀俄明州，CWD已逐渐蔓延至骡鹿（Odocoileus hemionus）种群，形成了可用于评估选择压力的疾病史自然变异。本研究借助空间变异与新型时间对比分析，探究了CWD与骡鹿朊蛋白基因225位密码子突变（可减缓疾病进展）之间的关联。研究发现，携带“缓发型”225F等位基因的个体CWD检测呈阳性的概率更低，且225F等位基因在暴露于CWD更久的鹿群中更为常见。此外，我们还发现，在过去二十年中，CWD感染率更高的鹿群内，225F等位基因频率的增幅更为显著。本研究通过分析个体与鹿群层面的疾病数据时空分布模式，拓展了既往研究范畴，为自由活动的野生动物中的疾病驱动选择提供了多维度证据。