Strain diversity and spatial distribution are linked to epidemic dynamics in host populations

The inherently variable nature of epidemics renders predictions of when and where infection is expected to occur challenging. Differences in pathogen strain composition, diversity, fitness, and spatial distribution are generally ignored in epidemiological modeling and are rarely studied in natural populations, yet they may be important drivers of epidemic trajectories. To examine how these factors are linked to epidemics in natural host populations, we collected epidemiological and genetic data from fifteen populations of the powdery mildew fungus, Podosphaera plantaginis, on Plantago lanceolata in the Åland Islands, Finland. In each population, we tracked spatiotemporal disease progression throughout one epidemic season and coupled our survey of infection with intensive field sampling of the pathogen. We found that strain composition varied greatly among populations in the landscape. Within populations, strain composition was driven by the sequence of strain activity: early-active strains reached higher abundances, leading to consistent strain compositions over time. Co-occurring strains also varied in their contribution to the growth of the local epidemic, and these fitness inequalities were linked to epidemic dynamics: a higher proportion of hosts became infected in populations containing strains that were more similar in fitness. Epidemic trajectories in the populations were also linked to strain diversity and to spatial dynamics: higher infection rates occurred in populations containing higher strain diversity, while spatially-clustered epidemics experienced lower infection rates. Together, our results suggest that spatial and/or temporal variation in strain composition, diversity, and fitness of pathogen populations are important factors generating variation in epidemiological trajectories among infected host populations. Methods We collected epidemiological and genetic data from fifteen populations of the powdery mildew fungus, Podosphaera plantaginis, on Plantago lanceolata in the Åland Islands, Finland. In each population, we tracked spatiotemporal disease progression throughout one epidemic season and coupled our survey of infection with intensive field sampling of the pathogen. Pathogen samples were assigned multi-locus genotypes ("strains") using a SNP panel.流行病的内在变异性使得预测感染发生的时间与地点极具挑战。病原体菌株组成、多样性、适合度及空间分布的差异，在流行病学建模中通常被忽略，在自然种群中也鲜有研究，但它们或许是驱动流行病传播轨迹的关键因素。为探究这些因素与自然宿主种群流行病之间的关联，我们于芬兰奥兰群岛的长叶车前（*Plantago lanceolata*）上，采集了15个白粉菌（*Podosphaera plantaginis*）种群的流行病学与遗传学数据。在每个种群中，我们追踪了一个流行病季内的时空疾病进展，并将感染调查与对病原体的密集野外采样相结合。 研究发现，景观中不同种群的菌株组成差异显著。种群内部，菌株组成由菌株活动时序决定：早活跃菌株的丰度更高，使得随时间推移的菌株组成保持稳定。同时共存的菌株对局部流行病增长的贡献亦存在差异，这类适合度差异与流行病动态相关：在菌株适合度更为相似的种群中，宿主感染比例更高。种群的流行病轨迹还与菌株多样性及空间动态相关：菌株多样性更高的种群感染率也更高，而空间聚集性流行病的感染率则更低。综合来看，我们的结果表明，病原体种群的菌株组成、多样性与适合度的空间和/或时间变异，是导致受感染宿主种群间流行病学轨迹产生差异的重要因素。 ## 方法 我们在芬兰奥兰群岛的长叶车前（*Plantago lanceolata*）上采集了15个白粉菌（*Podosphaera plantaginis*）种群的流行病学与遗传学数据。在每个种群中，我们追踪了一个流行病季内的时空疾病进展，并将感染调查与对病原体的密集野外采样相结合。研究人员通过单核苷酸多态性（Single Nucleotide Polymorphism, SNP）分型面板为病原体样本分配了多位点基因型（即"菌株"）。