The genomic determinants of adaptive evolution in a fungal pathogen

Abstract BackgroundAntagonistic host-pathogen co-evolution is a determining factor in the outcome of infection and shapes genetic diversity at the population level of both partners. Little is known about the overall genomic rate of evolution in pathogens or the molecular bases of rapid adaptation. Here we apply a population genomic approach to infer genome-wide patterns of selection among thirteen isolates of the fungal pathogen Zymoseptoria tritici. ResultsBased on whole genome alignments, we report extensive presence-absence polymorphisms of genes resulting from a high extent of within population karyotypic variation. We apply different test statistics based on the distribution of non-synonymous and synonymous polymorphisms (pN/pS) and substitutions (dN/dS) to estimate rates of adaptation and identify specific targets of selection. We report that the pN/pS ratio of sites under purifying selection negatively correlates with the local recombination rate, as expected under a scenario of background selection. Contrasting polymorphism and divergence with a closely related species, we estimate that 44% of substitutions in the proteome of Z. tritici are adaptive and we find that the rate of adaptation is positively correlated with recombination rate. The proportion of adaptive amino acid substitutions in genes encoding determinants of pathogenicity is as high as 68% underlining the importance of positive selection in the evolution of virulence-associated traits. Using a maximum likelihood approach and codon models of sequence evolution, we furthermore identify a set of 786 additional genes showing signatures of diversifying selection, which we find are preferentially located in region of high recombination rates. ConclusionsWe report a high rate of adaptive mutations in the genome of Z. tritici, in particular in genes involved in host-pathogen interactions. Furthermore, we identify a set of genes with signature of balancing / diversifying selection, which we find are related to secondary metabolism and host infection. Finally, we report a strong impact of recombination on the efficacy of purifying, adaptive and diversifying selection, suggesting pervasive effect of linked selection in the genome and thereby highlighting the importance of recombination in this pathogen species.