Genetic structure of the poplar rust fungus Melampsora larici-populina: Evidence for isolation by distance in Europe and recent founder effects overseas

Dispersal has a great impact on the genetic structure of populations, but remains difficult to estimate by direct measures. In particular, gradual and stochastic dispersal are often difficult to assess and to distinguish, although they have different evolutionary consequences. Plant pathogens, especially rust fungi, are suspected to display both dispersal modes, though on different spatial scales. In this study, we inferred dispersal capacities of the poplar rust fungus Melampsora larici-populina by examining the genetic diversity and structure of 13 populations from eight European and two overseas countries in the Northern hemisphere. M. larici-populina was sampled from both cultivated hybrid poplars and on the wild host, Populus nigra. The populations were analyzed with 11 microsatellite and 8 virulence markers. Although isolates displayed different virulence profiles according to the host plant, neutral markers revealed little population differentiation with respect to the type of host. This suggests an absence of reproductive isolation between populations sampled from cultivated and wild poplars. Conversely, studying the relationship between geographic and genetic structure allowed us to distinguish between isolation by distance (IBD) patterns and long distance dispersal (LDD) events. The European populations exhibited a significant IBD pattern, suggesting a regular and gradual dispersal of the pathogen over this spatial scale. Nonetheless, the genetic differentiation between these populations was low, suggesting an important gene flow on a continental scale. The two overseas populations from Iceland and Canada were shown to result from rare LDD events, and exhibited signatures of strong founder effects. Furthermore, the high genetic differentiation between both populations suggested that these two recent introductions were independent. This study illustrated how the proper use of population genetics methods can enable contrasted dispersal modes to be revealed.

扩散对种群遗传结构具有显著影响，但通过直接观测手段对其进行量化仍颇具挑战。尤为关键的是，尽管渐进式扩散与随机扩散各自具有迥异的进化效应，但二者往往难以被评估与区分。植物病原菌，尤其是锈菌，被推测可同时采用这两种扩散模式，只是二者作用的空间尺度存在差异。本研究以杨树锈菌（Melampsora larici-populina）为研究对象，通过对北半球8个欧洲国家及2个海外国家共计13个种群的遗传多样性与遗传结构展开分析，推断该病原菌的扩散能力。该锈菌的采样宿主既包括栽培杂交杨，也包括野生寄主黑杨（Populus nigra）。研究团队采用11个微卫星标记与8个毒性标记对上述种群进行了遗传分析。尽管分离菌株的毒性谱因寄主植物不同而存在差异，但中性标记分析显示，基于寄主类型的种群遗传分化程度极低。这表明从栽培杨与野生杨中采样得到的种群之间不存在生殖隔离。反之，通过解析地理结构与遗传结构的关联特征，我们可区分距离隔离（isolation by distance, IBD）模式与长距离扩散（long distance dispersal, LDD）事件。欧洲种群呈现出显著的距离隔离模式，这表明该病原菌在该空间尺度下存在规律且渐进式的扩散行为。尽管如此，这些种群间的遗传分化程度仍较低，这暗示在大陆尺度上存在较强的基因流。来自冰岛与加拿大的两个海外种群被证实源于罕见的长距离扩散事件，且表现出显著的奠基者效应特征。此外，这两个海外种群间极高的遗传分化表明，这两次近期的种群引入事件彼此独立。本研究阐明了合理运用种群遗传学方法，可有效揭示不同类型的扩散模式。