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in the population-wide number of virulence types and (iii) – above all – the emergence of the cultivated population superseded the initial population which predominated at the same place before R7 resistance breakdown.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-寄生虫系统为红皇后（Red Queen）协同进化动态提供了极具说服力的例证。然而，范瓦伦（Van Valen）理论中强调的核心过程——军备竞赛动态可导致种群灭绝——迄今尚未被实证记录。造成这一现状的原因之一，或在于多数采样设计未能覆盖足够的时空尺度，无法阐明病原种群快速适应的进程。本研究通过25年时序采样，解析了一种植物病原菌——杨栅锈菌（Melampsora larici-populina）——的种群历史动态。1994年发生了一次关键适应性事件：自1982年起在西欧广泛种植的多个杨树品种所携带的R7抗病性（R7 resistance）被突破。对应的致病型随即在杨栅锈菌种群中快速扩散，甚至在感病寄主上也几乎在法国北部达到了固定频率。结合致病型谱的时序记录与种群遗传学时序数据，本研究的分析结果显示：其一，R7抗病性的突破催生了一个独特且同质化的遗传类群——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致病型个体的选择通过遗传搭车（hitchhiking）效应携带了多种其他致病型，最终导致种群整体的致病型数量显著上升；其三，也是最为关键的一点：栽培种群的出现取代了R7抗病性突破前在该区域占据主导的原初种群。本时序分析清晰展示了拮抗协同进化如何导致种群灭绝与更替，从而为红皇后动态核心的军备升级过程提供了直接实证依据。