The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.

病原体在新的或异质环境中的适应潜力是疾病流行风险的基础。生活史特征之间的拮抗多效性或差异资源分配可以限制病原体适应。然而，我们缺乏对个体性状的遗传结构如何产生权衡的理解。在这里，我们报告了一项基于全球 145 种小麦病原体小麦发酵酵母菌株的大规模研究来自四大洲。我们测量了 50 种生活史特征，包括对 12 种不同小麦宿主的毒力和繁殖以及对几种非生物胁迫的生长反应。为了阐明适应的遗传基础，我们使用了全基因组关联作图和遗传相关分析。我们表明大多数性状受多基因结构控制并且具有高度遗传性，这表明适应主要通过许多位点的等位基因频移进行。我们确定了与宿主定植和在压力环境中生存相关的性状之间的负遗传相关性。这种遗传限制表明多效性效应可能会限制病原体造成宿主损害的能力。相反，协同多效性可能促进了对非生物胁迫因素的适应。