INRA, UMR PaVé, B.P. 57, 42 rue Georges Morel, F49071 Beaucouzé, France.
Mol Ecol. 2011 Nov;20(21):4521-32. doi: 10.1111/j.1365-294X.2011.05288.x. Epub 2011 Oct 4.
Expanding global trade and the domestication of ecosystems have greatly accelerated the rate of emerging infectious fungal diseases, and host-shift speciation appears to be a major route for disease emergence. There is therefore an increased interest in identifying the factors that drive the evolution of reproductive isolation between populations adapting to different hosts. Here, we used genetic markers and cross-inoculations to assess the level of gene flow and investigate barriers responsible for reproductive isolation between two sympatric populations of Venturia inaequalis, the fungal pathogen causing apple scab disease, one of the fungal populations causing a recent emerging disease on resistant varieties. Our results showed the maintenance over several years of strong and stable differentiation between the two populations in the same orchards, suggesting ongoing ecological divergence following a host shift. We identified strong selection against immigrants (i.e. host specificity) from different host varieties as the strongest and likely most efficient barrier to gene flow between local and emerging populations. Cross-variety disease transmission events were indeed rare in the field and cross-inoculation tests confirmed high host specificity. Because the fungus mates within its host after successful infection and because pathogenicity-related loci prevent infection of nonhost trees, adaptation to specific hosts may alone maintain both genetic differentiation between and adaptive allelic combinations within sympatric populations parasitizing different apple varieties, thus acting as a 'magic trait'. Additional intrinsic and extrinsic postzygotic barriers might complete reproductive isolation and explain why the rare migrants and F1 hybrids detected do not lead to pervasive gene flow across years.
全球贸易的扩张和生态系统的驯化极大地加速了新发真菌感染性疾病的速度，而宿主转移物种形成似乎是疾病出现的主要途径。因此，人们越来越关注识别驱动适应不同宿主的种群之间生殖隔离进化的因素。在这里，我们使用遗传标记和交叉接种来评估基因流动水平，并研究导致苹果黑星病菌（Venturia inaequalis）两个同域种群之间生殖隔离的障碍，苹果黑星病菌是引起苹果黑星病的真菌病原体，是导致最近在抗性品种上出现的新兴疾病的真菌种群之一。我们的研究结果表明，在同一果园中，这两个种群在数年内保持着强烈而稳定的分化，这表明在宿主转移后，生态差异仍在继续。我们发现，来自不同宿主品种的移民（即宿主特异性）受到强烈选择，这是当地和新兴种群之间基因流动的最强且可能是最有效的障碍。事实上，田间跨品种疾病传播事件很少见，交叉接种试验也证实了宿主的高度特异性。由于真菌在成功感染后在其宿主内交配，并且与致病性相关的基因座阻止了非宿主树木的感染，因此对特定宿主的适应可能单独维持寄生在不同苹果品种上的同域种群之间的遗传分化和适应性等位基因组合，从而成为一种“神奇特征”。额外的内在和外在的合子后障碍可能会完成生殖隔离，并解释为什么检测到的稀有移民和 F1 杂种不会导致多年来的普遍基因流动。
