[Fungi • 2019] Megaphylogeny Resolves Global Patterns of Mushroom (Agaricomycetes) Evolution

 Phylogenetic relationships and diversification across 5,284 mushroom-forming fungi. 

in Varga, Krizsán, Földi, et al., 2019. 

   DOI: 10.1038/s41559-019-0834-1  

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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.

Fig. 1: Phylogenetic relationships and diversification across 5,284 mushroom-forming fungi.
One of the 245 analysed maximum-likelihood trees was randomly chosen and visualized. Trees were inferred from nrLSU, rpb2, ef1-a sequences with a phylogenomic backbone constraint of deep nodes. Branches are coloured by net diversification (speciation minus extinction) rate inferred in Bayesian Analysis of Macroevolutionary Mixtures (BAMM). Warmer colours denote a higher rate of diversification. Significant shifts in diversification rate are shown by triangles at nodes. Only shifts present on >50% of ten trees, with a Bayesian posterior probability >0.5 and a posterior odds ratio >5 are shown. See Supplementary Data 6 for detailed discussion of shifts. Reconstructed probabilities of ancestral plant hosts for order-level clades are shown as pie charts partitioned by the inferred ancestral probability for gymnosperm (green) and angiosperm host (black). Pie charts are given for the most recent common ancestors of each order plus backbone nodes within the Agaricales—for small orders see Supplementary Data 3. Inner and outer bars around the tree denote extant substrate preference (black, angiosperm; green, gymnosperm; grey, generalist) and the placement of species used for inferring the 650-gene phylogenomic backbone phylogeny. Geological time scale is indicated with grey/white concentric rings.

Torda Varga, Krisztina Krizsán, Csenge Földi, Bálint Dima, Marisol Sánchez-García, Santiago Sánchez-Ramírez, Gergely J. Szöllősi, János G. Szarkándi, Viktor Papp, László Albert, William Andreopoulos, Claudio Angelini, Vladimír Antonín, Kerrie W. Barry, Neale L. Bougher, Peter Buchanan, Bart Buyck, Viktória Bense, Pam Catcheside, Mansi Chovatia, Jerry Cooper, Wolfgang Dämon, Dennis Desjardin, Péter Finy, József Geml, Sajeet Haridas, Karen Hughes, Alfredo Justo, Dariusz Karasiński, Ivona Kautmanova, Brigitta Kiss, Sándor Kocsubé, Heikki Kotiranta, Kurt M. LaButti, Bernardo E. Lechner, Kare Liimatainen, Anna Lipzen, Zoltán Lukács, Sirma Mihaltcheva, Louis N. Morgado, Tuula Niskanen, Machiel E. Noordeloos, Robin A. Ohm, Beatriz Ortiz-Santana, Clark Ovrebo, Nikolett Rácz, Robert Riley, Anton Savchenko, Anton Shiryaev, Karl Soop, Viacheslav Spirin, Csilla Szebenyi, Michal Tomšovský, Rodham E. Tulloss, Jessie Uehling, Igor V. Grigoriev, Csaba Vágvölgyi, Tamás Papp, Francis M. Martin, Otto Miettinen, David S. Hibbett and László G. Nagy. 2019. Megaphylogeny Resolves Global Patterns of Mushroom Evolution. Nature Ecology & Evolution.  DOI: 10.1038/s41559-019-0834-1   

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