Coalescent-based delimitation and species-tree estimations reveal Appalachian origin and Neogene diversification in Russula subsection Roseinae

[Display omitted] •Coalescent species approach with phylogeny and morphology delimits cryptic species.•Novel clades discovered and phylogenetically resolved in a hyperdiverse clade.•The Appalachian Mountains are a refugial hotspot for Russula speciation.•Jump dispersal speciation is a common mode in ectomycorrhizal fungi.•Ectomycorrhizal species are able to track their host through fluctuating climate. Numerous lineages of mushroom-forming fungi have been subject to bursts of diversification throughout their evolutionary history, events that can impact our ability to infer well-resolved phylogenies. However, groups that have undergone quick genetic change may have the highest adaptive potential. As the second largest genus of mushroom-forming fungi, Russula provides an excellent model for studying hyper-diversification and processes in evolution that drives it. This study focuses on the morphologically defined group – Russula subsection Roseinae. Species hypotheses based on morphological differentiation and multi-locus phylogenetic analyses are tested in the Roseinae using different applications of the multi-species coalescent model. Based on this combined approach, we recognize fourteen species in Roseinae including the Albida and wholly novel Magnarosea clades. Reconstruction of biogeographic and host association history suggest that parapatric speciation in refugia during glacial cycles of the Pleistocene drove diversification within the Roseinae, which is found to have a Laurasian distribution with an evolutionary origin in the Appalachian Mountains of eastern North America. Finally, we detect jump dispersal at a continental scale that has driven diversification since the most recent glacial cycles.