Historic transposon mobilisation waves create distinct pools of adaptive variants in a major crop pathogen

Transposable elements (TEs) can drive the evolution of host-pathogen interactions and gains in antimicrobial resistance. However, how adaptive TEs arise in populations and historical contingencies affect TE dynamics remains unknown. Fungal pathogens in agriculture provide unique frameworks to address such questions due to the availability of spatially explicit sampling and well-characterized niche conditions. We characterised TE evolutionary dynamics using an extensive intraspecies sampling of 1,953 genomes across the global distribution range of the major fungal wheat pathogen Zymoseptoria tritici . Employing a pangenomic approach, we characterise genomic diversity and benchmark methods to robustly infer TE insertion polymorphism, before systematically assessing TEs as a source of adaptive variation. We annotated ∼3.2 million TE loci among genomes, finding substantial variation in TE content within and among populations. TE activity surged during the pathogen’s expansion from its centre of origin in the Middle East, with unique TE activity profiles arising in derived populations. TE-mediated adaptation emerged from distinct waves of TE mobilization. The highest rates of TE activity were observed over timescales as short as 25 years. 45 TE loci showing local adaptation signatures within 1kb of 49 host genes were identified, with adaptive TE insertions likely related to adaptation to antifungals and the plant host environment. This work highlights the power of vast genomic datasets to unravel intraspecies TE invasion histories and pinpoint factors likely driving recent adaptation. This argues for a shift in focus to incorporate deep population-level TE activity surveys in our pursuit to uncover the molecular drivers of adaptive evolution.