Analysis of genetic diversity and population structure of Epichloe fungal pathogens using pairwise population sampling of sibling species Epichloe typhina and Epichloe clarkii. Epichloe population genomics

Understanding the population genetic processes driving the evolution of plant pathogens is of central interest to plant pathologists and evolutionary biologists alike. However, most studies focus on host-pathogen associations in agricultural systems of high genetic and environmental homogeneity and less is known about the genetic structure of pathogen populations infecting wild plants in natural ecosystems. We performed parallel population sampling of two pathogenic Epichloe species occurring sympatrically on different host grasses in natural and seminatural grasslands in Europe: E. typhina infecting Dactylis glomerata and E. clarkii infecting Holcus lanatus. We sequenced 422 haploid isolates and generated genome-wide SNP datasets to investigate genetic diversity and population structure. Clustering analyses showed that in both species geographically separated populations formed genetically distinct groups which could result from local adaptation generating and maintaining genetic structure, however, separation between populations was less clear in E. typhina compared to E. clarkii. The patterns of among population admixture differed between species across the same geographic range: We found higher levels of genetic differentiation between populations and a stronger effect of isolation by distance in E. clarkii consistent with lower levels of gene flow compared to E. typhina. This pattern may be explained by the different dispersal abilities of the two pathogens and is expected to be influenced by the genetic structure of host populations. Furthermore, the overall higher genetic diversity within E. typhina populations compared to E. clarkii indicate highly different effective population sizes and suggest that evolutionary processes such as genetic drift and selection may have differentially affected populations in the two species. Our population genomic analyses provide insights into the factors contributing to population divergence of plant pathogens in natural systems and reveal a strong geographic structure in Epichloe which is likely driven by coevolutionary dynamics between host and pathogen at the local scale.