Genomic patterns and the evolutionary origin of an invasive fungal pathogen (Hymenoscyphus fraxineus) in Europe

Abstract

In the 1990s, a highly pathogenic and invasive lineage of the Asian ascomycete Hymenoscyphus fraxineus appeared in Europe. Spreading across the continent, the fungal lineage devastates common ash (Fraxinus excelsior) populations and is a threat to ash species worldwide.In contrast to highly diverse reference populations in Japan and East Russia, the expanding European population is characterized by the persistence of a mosaic of two ancestral haplotypes, and presumed constraints to recombination. Four hypotheses were proposed for the evolutionary origin of the European lineage. The first hypothesis H1 states that two, and only two, pathogenic founder individuals were transferred from Asia to Europe and successfully established. Alternatively, in addition to the fungus arriving in Europe, a change in function might have occurred and only then the lineage became invasive. The cause of such a change might have been H2: one to two mutations during meiosis; H3: the lateral transfer of a European cytoplasmatic element modifying the behavior of H. fraxineus; or H4: a hybridization event with a closely related European ascomycete.Only the hybridization hypothesis seems to explain all of the genome-wide characteristics observed for the nuclear genome. Existing reconstructions of phylogenetic relationships at different taxonomic levels provide the evolutionary context of the lineages potentially involved. Vital information was gained from three configurations of nucleotide diversity and population differentiation associated with the genomic mosaic of monomorphic tracts and diversity islands.This synthesis points to the importance of identifying the taxonomic and geographic origins of the conserved two genomic ancestries within the European lineage of H. fraxineus and of reconstructing the mosaic of ancestral parental haplotypes (ancestry blocks) across the genome. Only with this information at hand will it be possible, to reliably interpret population-genomic data in the search for the functional elements underlying this unbalanced host-pathogen system.