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The genomic determinants of adaptive evolution in a fungal pathogen

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Grandaubert,  Jonathan
Max Planck Fellow Group Environmental Genomics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Dutheil,  Julien Y.
Research Group Molecular Systems Evolution, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;
Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Stukenbrock,  Eva H.
Max Planck Fellow Group Environmental Genomics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Citation

Grandaubert, J., Dutheil, J. Y., & Stukenbrock, E. H. (2019). The genomic determinants of adaptive evolution in a fungal pathogen. Evolution Letters, 3(3), 299-312. doi:10.1002/evl3.117.


Cite as: https://hdl.handle.net/21.11116/0000-0003-7056-E
Abstract
Antagonistic host-pathogen co-evolution is a determining factor in the outcome of infection and shapes genetic diversity at the population level of both partners. While the molecular function of an increasing number of genes involved in pathogenicity is being uncovered, little is known about the molecular bases and genomic impact of hst-pathogen coevolution and 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. Using whole genome alignments, we characterize intragenic polymorphism, and we apply different test statistics based on the distribution of non-synonymous and synonymous polymorphisms (pN/pS) and substitutions (dN/dS) to (1) characterise the selection regime acting on each gene, (2) estimate rates of adaptation and (3) identify targets of selection. We correlate our estimates with different genome variables to identify the main determinants of past and ongoing adaptive evolution, as well as purifying and balancing selection. We report a negative relationship between pN/pS and fine-scale recombination rate and a strong positive correlation between the rate of adaptive non-synonymous substitutions (ωa) and recombination rate. This result suggests a pervasive role of Hill-Robertson interference even in a species with an exceptionally high recombination rate (60 cM/Mb). Moreover, we report that the genome-wide fraction of adaptive non-synonymous substitutions (α) is ~ 44%, however in genes encoding determinants of pathogenicity we find a mean value of alpha ~ 68% demonstrating a considerably faster rate of adaptive evolution in this class of genes. We identify 787 candidate genes under balancing selection with an enrichment of genes involved in secondary metabolism and host infection, but not predicted effectors. This suggests that different classes of pathogenicity-related genes evolve according to distinct selection regimes. Overall our study shows that sexual recombination is a main driver of genome evolution in this pathogen.