Data from: The escalatory red queen: population extinction and replacement following arms-race dynamics in poplar rust

Host-parasite systems provide convincing examples of Red Queen co-evolutionary dynamics. Yet, a key process underscored in Van Valen’s theory, that arms-race dynamics can result in extinction, has never been documented. One reason for this may be that most sampling designs lack the breadth needed to illuminate the rapid pace of adaptation by pathogen populations. In this study we used a 25-years temporal sampling to decipher the demographic history of a plant pathogen: the poplar rust fungus, Melampsora larici-populina. A major adaptive event occurred in 1994 with the breakdown of R7 resistance carried by several poplar cultivars widely planted in Western Europe since 1982. The corresponding virulence rapidly spread in M. larici-populina populations, and nearly reached fixation in northern France, even on susceptible hosts. Using both temporal records of virulence profiles and temporal population genetic data, our analyses revealed that (i) R7 resistance breakdown resulted in the emergence of a unique and homogeneous genetic group, the so-called cultivated population, which predominated in northern France for about 20 years, (ii) selection for Vir7 individuals brought with it multiple other virulence types via hitch-hiking, resulting in an overall increase in the population-wide number of virulence types and (iii) – above all – the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown. Our temporal analysis illustrates how antagonistic co-evolution can lead to population extinction and replacement, hence providing direct evidence for the escalation process which is at the core of Red Queen dynamics.

宿主-寄生物系统（host-parasite systems）为红皇后协同进化动态（Red Queen co-evolutionary dynamics）提供了极具说服力的实证案例。然而，范瓦伦理论（Van Valen's theory）中强调的一项核心过程——军备竞赛动态可引发物种灭绝——却始终未被观测记录。究其根源，多数采样设计的覆盖广度不足以揭示病原菌种群快速的适应进程，或是该现象未被记录的重要原因。本研究依托长达25年的时间序列采样，解析了一种植物病原菌——杨树叶锈菌（*Melampsora larici-populina*）——的种群历史动态。1994年，该病原菌种群发生了一次重大适应事件：自1982年起在西欧广泛种植的多个杨树栽培品种所携带的R7抗性（R7 resistance）被其突破。对应的毒力型在杨树叶锈菌种群中快速扩散，甚至在感病寄主上，该毒力型也几乎在法国北部的种群中达到了固定频率。结合毒力型谱的时序记录与种群遗传数据，我们的分析揭示了三项核心结论：（i）R7抗性突破催生了一个独特且遗传均一的类群，即所谓的"栽培种群"，该类群在法国北部占据主导地位长达约20年；（ii）对携带Vir7毒力的个体的选择通过遗传搭车效应（hitch-hiking）连带引入了多种其他毒力型，进而导致种群整体的毒力型数量显著上升；（iii）尤为关键的是，该栽培种群的出现取代了R7抗性突破前在同一区域占据主导的初始种群。本时间序列分析阐明了拮抗协同进化如何引发种群灭绝与替代，从而为红皇后动态核心的军备升级过程提供了直接的实证证据。