Phylogenetic Relationships, Speciation, and Origin of Armillaria in the Northern Hemisphere: A Lesson Based on rRNA and Elongation Factor 1-Alpha

Armillaria species have a global distribution and play various roles in the natural ecosystems, e.g., pathogens, decomposers, and mycorrhizal associates. However, their taxonomic boundaries, speciation processes, and origin are poorly understood. Here, we used a phylogenetic approach with 358 samplings from Europe, East Asia, and North America to delimit the species boundaries and to discern the evolutionary forces underpinning divergence and evolution. Three species delimitation methods indicated multiple unrecognized phylogenetic species, and biological species recognition did not reflect the natural evolutionary relationships within Armillaria; for instance, biological species of A. mellea and D. tabescens are divergent and cryptic species/lineages exist associated with their geographic distributions in Europe, North America, and East Asia. While the species-rich and divergent Gallica superclade might represent three phylogenetic species (PS I, PS II, and A. nabsnona) that undergo speciation. The PS II contained four lineages with cryptic diversity associated with the geographic distribution. The genus Armillaria likely originated from East Asia around 21.8 Mya in early Miocene when Boreotropical flora (56–33.9 Mya) and the Bering land bridge might have facilitated transcontinental dispersal of Armillaria species. The Gallica superclade arose at 9.1 Mya and the concurrent vicariance events of Bering Strait opening and the uplift of the northern Tibetan plateau might be important factors in driving the lineage divergence.