The evolution of ectomycorrhizal symbiosis and host-plant switches are the main drivers for diversification of Amanitaceae (Agaricales, Basidiomycota).

Background: Evolutionary radiation is widely recognized as a mode of species diversification, but the drivers of the rapid diversification of fungi remain largely unknown. Here, we used Amanitaceae, one of the most diverse families of macro-fungi, to investigate the mechanism underlying its diversification.

Results: The ancestral state of the nutritional modes was assessed based on phylogenies obtained from fragments of 36 single-copy genes and stable isotope analyses of carbon and nitrogen. Moreover, a number of time-, trait-, and paleotemperature-dependent models were employed to investigate if the acquisition of ectomycorrhizal (ECM) symbiosis and climate changes promoted the diversification of Amanitaceae. The results indicate that the evolution of ECM symbiosis has a single evolutionary origin in Amanitaceae. The earliest increase in diversification coincided with the acquisition of the ECM symbiosis with angiosperms in the middle Cretaceous. The recent explosive diversification was primarily triggered by the host-plant switches from angiosperms to the mixed forests dominated by Fagaceae, Salicaceae, and Pinaceae or to Pinaceae.

Conclusions: Our study provides a good example of integrating phylogeny, nutritional mode evolution, and ecological analyses for deciphering the mechanisms underlying fungal evolutionary diversification. This study also provides new insights into how the transition to ECM symbiosis has driven the diversification of fungi.