Megaphylogeny resolves global patterns of mushroom evolution
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
30886374
PubMed Central
PMC6443077
DOI
10.1038/s41559-019-0834-1
PII: 10.1038/s41559-019-0834-1
Knihovny.cz E-resources
- MeSH
- Agaricales genetics MeSH
- Phylogeny MeSH
- Genetic Variation MeSH
- Genome, Fungal * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
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.
Biodiversity Unit Finnish Environment Institute Helsinki Finland
Botanical Museum University of Helsinki Helsinki Finland
Center for Forest Mycology Research Northern Research Station US Forest Service Madison WI USA
Clark University Worcester MA USA
Damjanich u 54 Budapest Hungary
Department of Biology Microbiology Utrecht University Utrecht the Netherlands
Department of Biology San Francisco State University San Francisco CA USA
Department of Biology University of Central Oklahoma Edmond OK USA
Department of Botany Faculty of Horticultural Science Szent István University Budapest Hungary
Department of Botany Moravian Museum Brno Czech Republic
Department of Cryptogamic Botany Swedish Museum of Natural History Stockholm Sweden
Department of Ecology and Evolutionary Biology University of Tennessee Knoxville TN USA
Department of Ecology and Evolutionary Biology University of Toronto Toronto Ontario Canada
Department of Microbiology Faculty of Science and Informatics University of Szeged Szeged Hungary
Department of Mycology W Szafer Institute of Botany Polish Academy of Sciences Kraków Poland
Department of Plant Anatomy Institute of Biology Eötvös Loránd University Budapest Hungary
Department of Plant and Microbial Biology University of California Berkeley Berkeley CA USA
Faculty of Forestry and Wood Technology Mendel University in Brno Brno Czech Republic
Herbarium Rooseveltensis Amanitarum Roosevelt NJ USA
Hungarian Mycological Society Budapest Hungary
Institute of Ecology and Earth Sciences University of Tartu Tartu Estonia
Institute of Plant and Animal Ecology Russian Academy of Sciences Ekaterinburg Russia
Instituto de Micología y Botánica CONICET Universidad de Buenos Aires Buenos Aires Argentina
Jardin Botanico Nacional Ma Moscoso Santo Domingo Dominican Republic
Manaaki Whenua Landcare Research Auckland New Zealand
Manaaki Whenua Landcare Research Lincoln New Zealand
MTA SZTE 'Lendulet' Fungal Pathogenicity Mechanisms Research Group Szeged Hungary
Natural History Museum Slovak National Museum Bratislava Slovakia
Naturalis Biodiversity Center Leiden the Netherlands
Oberfeldstraße 9 St Georgen bei Salzburg Austria
Plant and Microbial Biology University of California Berkeley CA USA
Section for Genetics and Evolutionary Biology University of Oslo Oslo Norway
State Herbarium of South Australia Adelaide South Australia Australia
The Jodrell Laboratory Royal Botanic Gardens Kew UK
The New York Botanical Garden New York NY USA
US Department of Energy Joint Genome Institute Walnut Creek CA USA
See more in PubMed
Jetz W, Pyron RA. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol. 2018;2:850–858. PubMed
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. The global diversity of birds in space and time. Nature. 2012;491:444–448. PubMed
Rabosky DL, et al. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat Commun. 2013;4 1958. PubMed
Alfaro ME, et al. Explosive diversification of marine fishes at the Cretaceous–Palaeogene boundary. Nat Ecol Evol. 2018;2:688–696. PubMed
Alfaro ME, et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci U S A. 2009;106:13410–4. PubMed PMC
Nagy LG, et al. The evolution of defense mechanisms correlate with the explosive diversification of autodigesting coprinellus mushrooms (agaricales, fungi) Syst Biol. 2012;61:595–607. PubMed
Wilson AW, Hosaka K, Mueller GM. Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria. New Phytol. 2017;213:1862–1873. PubMed PMC
Wilson AW, Binder M, Hibbett DS. Diversity and evolution of ectomycorrhizal host associations in the sclerodermatineae (Boletales, Basidiomycota) New Phytol. 2012;194:1079–1095. PubMed
Sánchez-Ramírez S, Tulloss RE, Amalfi M, Moncalvo JM. Palaeotropical origins, boreotropical distribution and increased rates of diversification in a clade of edible ectomycorrhizal mushrooms (Amanita section Caesareae) J Biogeogr. 2015;42:351–363.
Sánchez-Garcia M, Matheny PB. Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom-forming fungi? A case study in the Tricholomatineae (Agaricales) Evolution (N. Y) 2017;71:51–65. PubMed
Wilson AW, Binder M, Hibbett DS. Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis. Evolution (N. Y) 2011;65:1305–1322. PubMed
Hibbett DS. After the gold rush, or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century. Mycol Res. 2007;111:1001–1018. PubMed
Hibbett DS. Trends in morphological evolution in homobasidiomycetes inferred using maximum likelihood: A comparison of binary and multistate approaches. Syst Biol. 2004;53:889–903. PubMed
Hibbett DS, Binder M. Evolution of complex fruiting-body morphologies in homobasidiomycetes. Proc Biol Sci. 2002;269:1963–1969. PubMed PMC
Matheny PB, et al. Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia. 2006;98:982–95. PubMed
Kirk P, Cannon P, Minter D, S J. Dictionaty of the Fungi. CABI International; 2011. DOI
Floudas D, et al. The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes. Science (80-. ) 2012;336:1715–1719. PubMed
Kohler A, et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat Genet. 2015;47:410–415. PubMed
Lutzoni F, et al. Contemporaneous radiations of fungi and plants linked to symbiosis. Nat Commun. 2018;9 5451. PubMed PMC
Rabosky DL. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One. 2014;9 PubMed PMC
McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD. Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci U S A. 2009;106:7083–8. PubMed PMC
Looney BP, Ryberg M, Hampe F, Sánchez-García M, Matheny PB. Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi. Mol Ecol. 2016;25:630–647. PubMed
Krah F-S, et al. Evolutionary dynamics of host specialization in wood-decay fungi. BMC Evol Biol. 2018;18:119. PubMed PMC
Beaulieu JM, O’Meara BC. Extinction can be estimated from moderately sized molecular phylogenies. Evolution (N. Y) 2015;69:1036–1043. PubMed
Rabosky DL. Challenges in the estimation of extinction from molecular phylogenies: A response to Beaulieu and O’Meara. Evolution (N. Y) 2016;70:218–228. PubMed
Rabosky DL. Extinction rates should not be estimated from molecular phylogenies. Evolution (N. Y) 2010;64:1816–1824. PubMed
May MR, Hohna S, Moore BR. A Bayesian approach for detecting the impact of mass-extinction events on molecular phylogenies when rates of lineage diversification may vary. Methods Ecol Evol. 2016;7:947–959.
Tennant JP, Mannion PD, Upchurch P, Sutton MD, Price GD. Biotic and environmental dynamics through the Late Jurassic-Early Cretaceous transition: evidence for protracted faunal and ecological turnover. Biol Rev. 2017;92:776–814. PubMed PMC
Casadevall A. Fungi and the Rise of Mammals. PLoS Pathog. 2012;8:e1002808. PubMed PMC
Vajda V, McLoughlin S. Fungal Proliferation at the Cretaceous-Tertiary Boundary. Science (80-. ) 2004;303:1489–1489. PubMed
Mittelbach GG, et al. Evolution and the latitudinal diversity gradient: Speciation, extinction and biogeography. Ecology Letters. 2007;10:315–331. PubMed
Peay KG, Kennedy PG, Talbot JM. Dimensions of biodiversity in the Earth mycobiome. Nat Rev Microbiol. 2016;14:434–447. PubMed
Shi L-L, et al. Variation in forest soil fungal diversity along a latitudinal gradient. Fungal Divers. 2014;64:305–315.
Tedersoo L, et al. Global diversity and geography of soil fungi. Science (80-. ) 2014;346:1256688–1256688. PubMed
Sánchez-Ramírez S, Etienne RS, Moncalvo JM. High speciation rate at temperate latitudes explains unusual diversity gradients in a clade of ectomycorrhizal fungi. Evolution (N. Y) 2015;69:2196–2209. PubMed
Gavrilets S, Losos JB. Adaptive radiation: Contrasting theory with data. Science. 2009;323:732–737. PubMed
Givnish TJ. Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: Why conceptual distinctions are fundamental to understanding evolution. New Phytol. 2015;207:297–303. PubMed
Maddison WP, Midford PE, Otto SP. Estimating a binary character’s effect on speciation and extinction. Syst Biol. 2007;56:701–710. PubMed
Fitzjohn RG. Diversitree: Comparative phylogenetic analyses of diversification in R. Methods Ecol Evol. 2012;3:1084–1092.
Berendse F, Scheffer M. The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery’. Ecol Lett. 2009;12:865–72. PubMed PMC
Niklas KJ, Tiffney BH, Knoll AH. Patterns in vascular land plant diversification. Nature. 1983;303:614–616.
Berner RA. Phanerozoic atmospheric oxygen: New results using the GEOCARBSULF model. Am J Sci. 2009;309:603–606.
Staden R. The Staden sequence analysis package. Mol Biotechnol. 1996;5:233–241. PubMed
CABI. Species Fungorum. Royal Botanic Gardens Kew. 2018
Knudsen H, V J. Funga Nordica. 2008
Loytynoja A, Goldman N. Phylogeny-Aware Gap Placement Prevents Errors in Sequence Alignment and Evolutionary Analysis. Science (80-. ) 2008;320:1632–1635. PubMed
Loytynoja A, Goldman N. From The Cover: An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci. 2005;102:10557–10562. PubMed PMC
Tóth A, et al. Iteratively Refined Guide Trees Help Improving Alignment and Phylogenetic Inference in the Mushroom Family Bolbitiaceae. PLoS One. 2013;8 PubMed PMC
Gnerre S, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci. 2011;108:1513–1518. PubMed PMC
Martin J, et al. Rnnotator: An automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads. BMC Genomics. 2010;11 PubMed PMC
Chin C-S, et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 2016;13:1050–1054. PubMed PMC
Lam K-K, LaButti K, Khalak A, Tse D. FinisherSC: a repeat-aware tool for upgrading de novo assembly using long reads. Bioinformatics. 2015;31:3207–3209. PubMed
Grigoriev IV, et al. MycoCosm portal: Gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42 PubMed PMC
Darling A, Carey L, Feng W. The Design, Implementation, and Evaluation of mpiBLAST. 4th Int. Conf. Linux Clust. HPC Revolut. 2003 conjunction with Clust. Conf. Expo; 2003.
van Dongen S. Graph Stimul by flow Clust. PhD thesis, University of Utrecht; 2000. Graph clustering by flow simulation.
Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–577. PubMed
Nagy LG, et al. Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Mol Biol Evol. 2016;33:959–970. PubMed
Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. PubMed PMC
Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–593. PubMed PMC
Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25:2286–2288. PubMed
Åkerborg Ö, Sennblad B, Lagergren J. Birth-death prior on phylogeny and speed dating. BMC Evol Biol. 2008;8 PubMed PMC
Smith SY, Currah RS, Stockey RA. Cretaceous and Eocene poroid hymenophores from Vancouver Island, British Columbia. Mycologia. 2004;96:180–186. PubMed
Hibbett DS, Grimaldi D, Donoghue MJ. Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of homobasidiomycetes. Am J Bot. 1997;84:981–991. PubMed
Poinar G. Bird’s nest fungi (Nidulariales: Nidulariaceae) in Baltic and Dominican amber. Fungal Biol. 2014;118:325–329. PubMed
Brown RW. A bracket fungus from the late Tertiary of southwestern Idaho. Journal of the Washington Academy of Sciences. 30:422–424.
Magallon-Puebla S, Cevallos-Ferriz SRS. A fossil earthstar (Geasteraceae; Gasteromycetes) from the Late Cenozoic of Puebla, Mexico. Am J Bot. 1993;80:1162–1167.
Near TJ, Meylan PA, Shaffer HB. Assessing Concordance of Fossil Calibration Points in Molecular Clock Studies: An Example Using Turtles. Am Nat. 2005;165:137–146. PubMed
Charif D, Lobry JR. SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis. Springer; Berlin, Heidelberg: 2007. pp. 207–232. DOI
Camacho C, et al. BLAST+: Architecture and applications. BMC Bioinformatics. 2009;10:1–9. PubMed PMC
Sanderson MJ. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol. 2002;19:101–109. PubMed
Yang Z. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586–1591. PubMed
Thorne JL, Kishino H, Painter IS. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol. 1998;15:1647–1657. PubMed
Bodensteiner P, Binder M, Moncalvo JM, Agerer R, S. Hibbett D. Phylogenetic relationships of cyphelloid homobasidiomycetes. Mol Phylogenet Evol. 2004;33:501–515. PubMed
Holt BG, et al. An Update of Wallace’s Zoogeographic Regions of the World. Science (80-. ) 2013;339:74–78. PubMed
Core Team R. R: A language and environment for statistical computing. 2018.
Fitzjohn RG. Quantitative traits and diversification. Syst Biol. 2010;59:619–633. PubMed
Goldberg EE, Lancaster LT, Ree RH. Phylogenetic inference of reciprocal effects between geographic range evolution and diversification. Syst Biol. 2011;60:451–465. PubMed
Pagel M, Meade A. BayesTraits. 2007;2 URL [ http//www.Evol.rdg.ac.uk/BayesTraits.
Pagel M. Inferring the historical patterns of biological evolution. Nature. 1999;401:877–884. PubMed
Xie W, Lewis PO, Fan Y, Kuo L, Chen MH. Improving marginal likelihood estimation for bayesian phylogenetic model selection. Syst Biol. 2011;60:150–160. PubMed PMC
Revell LJ. phytools: An R package for phylogenetic comparative biology (and other things) Methods Ecol Evol. 2012;3:217–223.
Huelsenbeck JP, Nielsen R, Bollback JP. Stochastic mapping of morphological characters. Syst Biol. 2003;52:131–158. PubMed
Wickham H. Ggplot2. Elegant Graphics for Data Analysis. 2009 doi: 10.1007/978-0-387-98141-3. DOI
Paradis E, Claude J, Strimmer K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–290. PubMed
Fitzjohn RG, Maddison WP, Otto SP. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst Biol. 2009;58:595–611. PubMed
Rabosky DL, et al. BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol Evol. 2014;5:701–707.
Geweke J. Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments. Bayesian Stat. 1992;4:169–193. doi: 1176289.
Plummer M, Best N, Cowles K, Vines K. CODA: convergence diagnosis and output analysis for MCMC. R News. 2006;6:7–11.
Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL. AWTY (are we there yet?): A system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics. 2008;24:581–583. PubMed
Moore BR, Höhna S, May MR, Rannala B, Huelsenbeck JP. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. Proc Natl Acad Sci. 2016;113:9569–9574. PubMed PMC
Meyer ALS, Wiens JJ. Estimating diversification rates for higher taxa: BAMM can give problematic estimate of rates and rate shifts. Evolution (N. Y) 2017:1–15. doi: 10.1111/evo.13378. PubMed DOI
Magallon S, Sanderson MJ. Absolute diversification rates in angiosperms clades. Evolution (N. Y) 2001;55:1762–1780. PubMed
Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W. GEIGER: Investigating evolutionary radiations. Bioinformatics. 2008;24:129–131. PubMed
Höhna S. The time-dependent reconstructed evolutionary process with a key-role for mass-extinction events. J Theor Biol. 2015;380:321–331. PubMed
Höhna S. Fast simulation of reconstructed phylogenies under global time-dependent birth-death processes. Bioinformatics. 2013;29:1367–1374. PubMed
Hohna S, May MR, Moore BR. Phylogeny Simulation and Diversification Rate Analysis with TESS. 2015:1–98. https://cran.r-project.org/web/packages/TESS/vignettes/Bayesian_Diversification_Rate_Analysis.pdf.
Kass RE, Raftery AE. Bayes factors. J Am Stat Assoc. 1995;90:773–795.
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Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay