The rapid diversification of Boletales is linked to Early Eocene and Mid-Miocene Climatic Optima

SUMMARY Investigating the mechanisms that underpin the diversity and distribution patterns of species is fundamental in ecology and evolution. However, the study of fungi, particularly the ectomycorrhizal group, has been relatively constrained in this field. We conducted a high-resolution phylogenomic analysis of Boletales, an ecologically and economically significant group of fungi, covering 83 genera across 15 families. We subsequently investigated its evolutionary history using sequences at four genes obtained from 984 species across 121 genera within 15 families. The findings unveiled that Boletales likely originated in Early Jurassic and underwent two remarkable episodes of rapid diversification, commencing in early Eocene (∼54 Mya) and early Miocene (∼17 Mya) epochs. The notable surges were predominantly driven by ectomycorrhizal clades, with a specific emphasis on East Asia and North America. These expansions were strongly correlated with the warm-humid paleoclimates during the Early Eocene Climatic Optimum and Mid-Miocene Climatic Optimum, as well as the rapid expansion of Fagales and Pinaceae hosts. This study provides novel insights into the spatiotemporal evolution of fungi, highlighting the synergistic impact of abiotic factors, such as warm and humid paleoclimates, and the biotic factor of rapid diversification of host plants on the fungal diversification.