Megaphylogeny resolves global patterns of mushroom evolution

Torda Varga (1) , Krisztina Krizsán (1) , Csenge Földi (1) , Bálint Dima (2) , Marisol Sánchez-García (3) , Santiago Sánchez-Ramírez (4) , Gergely J Szöllősi (2) , János G Szarkándi (5) , Viktor Papp (6) , László Albert (7) , William Andreopoulos (8) , Claudio Angelini (9) , Vladimír Antonín (10) , Kerrie W Barry (8) , Neale L Bougher (11) , Peter Buchanan (12) , Bart Buyck (13, 14, 15) , Viktória Bense (1) , Pam Catcheside (16) , Mansi Chovatia (8) , Jerry Cooper (12) , Wolfgang Dämon , Dennis Desjardin (17) , Péter Finy , József Geml (18) , Sajeet Haridas (8) , Karen Hughes (19) , Alfredo Justo (3) , Dariusz Karasiński (20) , Ivona Kautmanova (21) , Brigitta Kiss (1) , Sándor Kocsubé (5) , Heikki Kotiranta (22) , Kurt M Labutti (8) , Bernardo E Lechner (23) , Kare Liimatainen (24) , Anna Lipzen (8) , Zoltán Lukács , Sirma Mihaltcheva (8) , Louis N Morgado (18, 25) , Tuula Niskanen (24) , Machiel E Noordeloos (18) , Robin A Ohm (26) , Beatriz Ortiz-Santana (27) , Clark Ovrebo (28) , Nikolett Rácz (5) , Robert Riley (8) , Anton Savchenko (29, 30) , Anton Shiryaev (31) , Karl Soop (32) , Viacheslav Spirin (29) , Csilla Szebenyi (5, 33) , Michal Tomšovský (34) , Rodham E Tulloss (35, 36) , Jessie Uehling (37) , Igor V Grigoriev (8, 37) , Csaba Vágvölgyi (5) , Tamás Papp (5, 30) , Francis Martin (38) , Otto Miettinen (29) , David S Hibbett (3) , László G Nagy (1)

1 MTA - Hungarian Academy of Sciences
2 ELTE - Eötvös Loránd University
3 Clark University
4 University of Toronto
5 University of Szeged [Szeged]
6 Szent István University
7 Hungarian Mycological Society
8 United States Department of Energy
9 Jardín Botánico Nacional Dr. Rafael Ma. Moscoso
10 Moravian Museum
11 Western Australian Herbarium
12 Manaaki Whenua – Landcare Research [Lincoln]
13 SU - Sorbonne Université
14 CNRS - Centre National de la Recherche Scientifique
15 ISYEB - Institut de Systématique, Evolution, Biodiversité
16 State Herbarium South Australia
17 SFSU - San Francisco State University
18 National Biodiversityt Center
19 University of Tennessee
20 PAN - Polska Akademia Nauk = Polish Academy of Sciences = Académie polonaise des sciences
21 Slovak National Museum
22 SYKE - Finnish Environment Institute
23 UBA - Universidad de Buenos Aires
24 Royal Botanic Gardens
25 UiO - University of Oslo
26 Universiteit Utrecht / Utrecht University [Utrecht]
27 US Forest Service
28 OU - University of Oklahoma
29 Helsingin yliopisto = Helsingfors universitet = University of Helsinki
30 University of Tartu
31 RAS - the Russian Academy of Sciences [Moscow, Russia]
32 NRM - Swedish Museum of Natural History
33 MTA Centre for Ecological Research
34 MENDELU - Mendel University in Brno
35 Herbarium Amanitarum Rooseveltensis
36 NYBG - New York Botanical Garden
37 UC Berkeley - University of California [Berkeley]
38 IAM - Interactions Arbres-Microorganismes

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.

Mots clés: PHYLOGENETIC ANALYSIS; FORMING FUNGI; EXPLOSIVE DIVERSIFICATION; ADAPTIVE RADIATION; EXTINCTION RATES; R PACKAGE; DIVERSITY; SPECIATION; LIKELIHOOD; BINARY; evolutionary history; phylogeny

Mots clés: histoire évolutive; arbre phylogénétique; basidiomycete; phylogénie; phylogénie moléculaire; champignon

Domaines: Sciences du Vivant [q-bio]

Torda Varga, Krisztina Krizsán, Csenge Földi, Bálint Dima, Marisol Sánchez-García, et al.. Megaphylogeny resolves global patterns of mushroom evolution. Nature Ecology & Evolution, 2019, 3 (4), pp.668-678. ⟨10.1038/s41559-019-0834-1⟩. ⟨hal-02352505⟩