The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen

Convergent evolution leads to identical phenotypic traits in different species or populations. Convergence can be driven by standing variation allowing selection to favour identical alleles in parallel or the same mutations can arise independently. However, the molecular basis of such convergent adaptation remains often poorly resolved. Pesticide resistance in agricultural ecosystems is a hallmark of convergence in phenotypic traits. Here, we analyse the major fungal pathogen Zymoseptoria tritici causing serious losses on wheat and with fungicide resistance emergence across several continents. We sampled three population pairs each from a different continent spanning periods early and late in the application of fungicides. To identify causal loci for resistance, we combined knowledge from molecular genetics work and performed genome-wide association studies (GWAS) on a global set of isolates. We discovered yet unknown factors in azole resistance including a gene encoding membrane associated functions. We found strong support for the hotspot model of resistance evolution with convergent changes in a small set of loci but additional loci showed more population-specific allele frequency changes. Genome-wide scans of selection showed that half of all known resistance loci were overlapping a selective sweep region. Hence, the application of fungicides was one of the major selective agents acting on the pathogen over the past decades. Furthermore, loci identified through GWAS showed the highest overlap with selective sweep regions underlining the importance to map phenotypic trait variation in evolving populations. Our population genomic analyses highlighted that both de novo mutations and gene flow contributed to convergent pesticide adaptation.

Automated summary

Convergent evolution was observed in pesticide resistance adaptation of the fungal pathogen Zymoseptoria tritici, with some loci showing convergent changes across populations while others displaying more population-specific allele frequency changes. Genome-wide association studies revealed unknown factors in azole resistance and showed that half of the known resistance loci overlapped with selective sweep regions, indicating the major selective pressure of fungicide application on the pathogen. Genomic analyses highlighted the contribution of both de novo mutations and gene flow to convergent pesticide adaptation.