Contrasting continental patterns of adaptive population divergence in a holarctic fungus

Abstract Understanding the population processes and genetic mechanisms that give rise to new species remains one of the most elusive goals of modern evolutionary biology. In the hyperdiverse and ecologically important Fungi, the process of speciation is virtually unknown, including for the more than 20,000 species of obligate ectomycorrhizal mutualists that play essential roles in ecosystem function. We investigated patterns of genome-wide differentiation in the ectomycorrhizal porcini mushroom Boletus edulis, a globally distributed species complex with broad ecological amplitude. By whole genome sequencing 160 individuals from across the Northern Hemisphere, we identified 792,923 SNPs and used these to elucidate the demographic and adaptive processes shaping global population differentiation. We show that B. edulis exhibits deeply contrasting patterns of genomic divergence between continents, with multiple lineages being present across North America, while a single lineage dominates Europe over a vast geographic scale. These geographical lineages are inferred to have diverged between 2.66 and 1.62 million years ago, corresponding to a period of climatic upheaval and the onset of glaciation during the Pliocene-Pleistocene boundary. High levels of genomic differentiation were observed among lineages despite evidence of substantial and ongoing introgression. Furthermore, genome scans, demographic inference and ecological niche models all suggest that genomic differentiation is maintained by environmental adaptation and not physical isolation. Our study uncovers striking differences on a truly global scale and emphasizes the importance of local adaptation and ecologically mediated divergence, rather than prezygotic barriers such as allopatry or genomic incompatibility in population differentiation in Fungi.