A population-level invasion by transposable elements in a fungal pathogen

Transposable elements (TEs) are key drivers of adaptive evolution within species. Yet, the propagation of TEs across the genome can be highly deleterious and ultimately lead to genome expansions. Hence, TE activity is likely under complex selection regimes within species. To address this, we analyzed a large whole-genome sequencing dataset of the fungal wheat pathogen Zymoseptoria tritici harboring TE-mediated adaptations to overcome host defenses and fungicides. We built a robust map of genome-wide TE insertion and deletion loci for six populations and 284 fungal individuals across the world. We identified a total of 29456 unfixed TE loci within the species and a significant excess of rare insertions indicating strong purifying selection. A subset of TEs recently swept to near complete fixation with at least one locus likely contributing to higher levels of fungicide resistance. TE-driven adaptation was also supported by evidence for selective sweeps. In parallel, we identified a substantial genome-wide expansion of TE families from the pathogen9s center of origin to more recently founded populations, suggesting that population bottlenecks played a major role in shaping TE content of the genome. The most dramatic expansion occurred among a pair of North American populations collected in the same field at an interval of 25 years. We show that both the activation of specific TEs and relaxed purifying selection likely underpin the expansion. Our study disentangles the effects of selection and TE bursts leading to intra-specific genome expansions, providing a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.