Standing genetic variation buffers field populations of Zymoseptoria tritici against seasonal and fungicide selection

Abstract

Zymoseptoria tritici is a fungal wheat pathogen whose exceptionally large effective population sizes and frequent sexual recombination enable rapid adaptation and the breakdown of disease control strategies, yet the relative contributions of demographic turnover and fungicide selection to within-season genomic change remain unresolved at the field scale. We analysed whole-genome sequences from five wheat fields sampled during epidemic progression, including paired untreated and fungicide-treated populations, to separate seasonal demographic change from fungicide effects on genome-wide diversity allowing us to compare minor allele frequency spectra and diversity statistics to disentangle these effectswithin individual fields. Field populations were locally differentiated yet nested within the broader European gene pool; within-season demographic turnover consistently shifted allele frequency spectra towards more shared, common alleles; whereas nucleotide diversity and adaptive potential remained largely unchanged. Seasonal demographic turnover accounted for most short-term genomic change, while fungicide effects were comparatively small, field-specific and acted primarily on pre-existing resistance alleles and standing genetic variation. Our results show that short-term adaptation is driven primarily by the redistribution rather than depletion of standing genetic variation, highlighting pathogen population biology as a key determinant of disease-control durability and emphasizing the value of population-informed genomic surveillance.