Radiation of mushroom-forming fungi correlates with novel modes of protecting sexual fruiting bodies.

The protection of vulnerable developing structures evolved repeatedly in terrestrial organisms and includes, among others, viviparity in animals and the seed in land plants. In mushroom-forming fungi (Agaricomycetes), sexual spores are born on fruiting bodies, the growth of which is a complex developmental process that is exposed to environmental factors (e.g., desiccation, fungivorous animals). Mushroom-forming fungi evolved a series of innovations in fruiting body protection, however, how these emerged is obscure, leaving the evolutionary principles of fruiting body development poorly known. Here, we show that developmental innovations that lead to the spore-producing surface (hymenophore) being enclosed in a protected environment display asymmetry in their evolution and are associated with increased diversification rates. 'Enclosed' development evolved convergently and became a dominant developmental type in several clades of mushrooms. This probably mirrors spore production benefits for species with protected fruiting body initials, by better coping with environmental factors. Our observations highlight new morphological traits associated with mushroom diversification that parallel the evolution of protection strategies in other organisms, such as viviparity or the seed in animals or plants, respectively, but in the context of spore development, highlighting the general importance of protecting vulnerable progeny across the tree of life.

Megaphylogeny resolves global patterns of mushroom evolution.

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.