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 hitchhiking, 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in the population-wide number of virulence types and (iii) – above all – the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown.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例证。然而，Van Valen理论中强调的一项核心过程——军备竞赛动态可引发物种灭绝——却从未被实证记录。造成这一空白的原因之一，或许是多数采样设计未能覆盖足够的时空广度，以阐明病原种群快速的适应进程。本研究依托长达25年的时序采样，解析了一种植物病原物：落叶松-杨栅锈菌（Melampsora larici-populina）的种群历史动态。1994年发生了一次重大适应事件：1982年起在西欧广泛种植的多个杨树品种所携带的R7抗病基因被突破。对应的毒性表型迅速在该锈菌种群中扩散，甚至在感病寄主上也几乎达到固定频率，在法国北部尤为显著。结合毒性表型的时序记录与种群遗传时序数据，本研究的分析揭示了三项核心发现：其一，R7抗病基因的突破催生了一个独特且遗传均一的遗传类群，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；其二，对Vir7毒性型的选择通过搭便车效应连带富集了多种其他毒性类型，最终导致种群整体的毒性类型总数整体上升；其三，尤为关键的是，该栽培种群的出现取代了R7抗病基因突破前在同一区域占主导的初始种群。本项时序分析直观展现了拮抗协同进化如何推动种群灭绝与替代，从而为红皇后协同进化动态核心的军备升级过程提供了直接实证依据。