Understanding the evolution of mushroom-forming fungi: macro-evolutionary analyses of a 5300-species phylogeny of Agaricomycetes

Torda Varga varga.torda@gmail.com ¹ Krisztina Krizsán ¹ János Gergő Szarkándi ² Bálint Dima ^3,4 Brigitta Kiss ¹ Csenge Földi ¹ Marisol Sánchez-García ⁶ Santiago Sánchez-Ramírez ⁷ Gergely J. Szöllősi ^8,9 David S. Hibbett ⁶ Csaba Vágvölgyi ² Tamás Papp ^2,5 László G. Nagy ¹

¹Institute of Biochemistry, Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary
²Department of Microbiology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary
³Department of Plant Anatomy, Eötvös Loránd University, Budapest, Hungary
⁴Department of Biosciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, Finland
⁵MTA-SZTE Fungal Pathogenicity Mechanisms Research Group, Department of Microbiology, Faculty of Science and Informatics, Hungarian Academy of Sciences, University of Szeged, Szeged, Hungary
⁶Biology Department, Clark University, Worcester, USA
⁷Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada
⁸Institute of Physics, Eötvös Loránd University, Budapest, Hungary
⁹MTA-ELTE “Lendulet” Evolutionary Genomics Research Group, Hungarian Academy of Science, Budapest, Hungary

The Agaricomycetes is one of the most morphologically and taxonomically diverse fungal lineages (comprised of >20000 species). It contains most of the iconic mushroom-forming fungi, yet, the macro-evolutionary mechanisms that have shaped its extant taxonomic and morphological diversity are barely known. To address this question, a large multigene phylogeny of Agaricomycetes was assembled, consisting of 5284 species and three loci (4835 nrLSU; 1253 RPB2 and 721 ef1-a sequences), including 1386 newly sequenced taxa. Maximum Likelihood trees were inferred along a phylogenomic backbone of 103 species and chronograms were estimated by applying temporal information of eight fungal fossils. Using BAMM (Bayesian Analysis of Macroevolutionary Mixtures) 40-60 core shifts (i.e. posterior-to-prior odds ratio ≥ 5) in diversification rate per tree were detected. Most core shifts were inferred in the Agaricales, suggesting that it has the largest speciation and extinction dynamics across Agaricomycete orders. Further, it was found that at least one mass extinction event has likely occurred during the evolution of the class (CoMET model and TESS analyses). Next, we investigated if morphological innovations found in fruiting bodies could underlie differences in diversification rate across Agaricomycete species. Some of the most typical evolutionary innovations of mushroom forming fungi are related to spore protection and propagation. Therefore it was tested whether three hallmark traits, the presence or absence of cap, the enlarged hymenial surface (by gills, pores, etc.) and the presence or absence of protective veil tissues have influenced diversification of the class. First the transition rates between character states (BayesTraits V.2.0) were estimated to reconstruct ancestral states and directionality in the evolution of these traits. This was followed by analyses of character state dependent diversification (BiSSE or MuSSE models), to test the effect of traits on species diversification. This study contributes to understanding the macro-evolutionary history of Agaricomycetes and to a better understanding of the evolution of mushroom-forming fungi.