Abstract
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.
Highlights
Explosive diversification events, with intermittent periods of relatively little change, have generated uneven patterns of species richness across the tree of life
Pileate-stipitate forms have arisen repeatedly from simpler morphologies during evolution[12,13,15] and dominate extant agaricomycete diversity (>21,000 described species16), but how this diversity arose, what explains the dominance of pileate-stipitate species in the class and whether fruiting body morphology impacts diversification rates are not known
This study represents a global analysis of the dynamic evolutionary history of mushroom-forming fungi
Summary
With intermittent periods of relatively little change, have generated uneven patterns of species richness across the tree of life. Studies of diversification of mushroom-forming fungi have focused on individual clades[6,7,8,9], yielding hypotheses on ecological opportunities[6], the evolution of mutualistic lifestyle[7,10] and fruiting body morphologies[6,11] as drivers of adaptive evolution in fungi. These inferences, based on specific clades, remained untested across larger phylogenetic scales. Pileate-stipitate forms have arisen repeatedly from simpler morphologies (for example, resupinate or coral-like) during evolution[12,13,15] and dominate extant agaricomycete diversity (>21,000 described species16), but how this diversity arose, what explains the dominance of pileate-stipitate species in the class and whether fruiting body morphology impacts diversification rates (for example, as a key innovation) are not known
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