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      Megaphylogeny resolves global patterns of mushroom evolution

      research-article
      1 , 1 , 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 9 , 13 , 14 , 15 , 1 , 16 , 9 , 17 , 18 , 19 , 20 , 21 , 9 , 22 , 3 , 23 , 24 , 1 , 6 , 25 , 9 , 26 , 27 , 9 , 28 , 9 , 21 , 27 , 21 , 29 , 30 , 31 , 6 , 9 , 32 , 33 , 34 , 32 , 6 , 35 , 36 , 37 , 9 , 38 , 6 , 6 , 39 , 32 , 3 , 1 , *
      Nature ecology & evolution

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          Abstract

          Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfill 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.

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          Most cited references65

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          Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.

          A latitudinal gradient in biodiversity has existed since before the time of the dinosaurs, yet how and why this gradient arose remains unresolved. Here we review two major hypotheses for the origin of the latitudinal diversity gradient. The time and area hypothesis holds that tropical climates are older and historically larger, allowing more opportunity for diversification. This hypothesis is supported by observations that temperate taxa are often younger than, and nested within, tropical taxa, and that diversity is positively correlated with the age and area of geographical regions. The diversification rate hypothesis holds that tropical regions diversify faster due to higher rates of speciation (caused by increased opportunities for the evolution of reproductive isolation, or faster molecular evolution, or the increased importance of biotic interactions), or due to lower extinction rates. There is phylogenetic evidence for higher rates of diversification in tropical clades, and palaeontological data demonstrate higher rates of origination for tropical taxa, but mixed evidence for latitudinal differences in extinction rates. Studies of latitudinal variation in incipient speciation also suggest faster speciation in the tropics. Distinguishing the roles of history, speciation and extinction in the origin of the latitudinal gradient represents a major challenge to future research.
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            AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics.

            A key element to a successful Markov chain Monte Carlo (MCMC) inference is the programming and run performance of the Markov chain. However, the explicit use of quality assessments of the MCMC simulations-convergence diagnostics-in phylogenetics is still uncommon. Here, we present a simple tool that uses the output from MCMC simulations and visualizes a number of properties of primary interest in a Bayesian phylogenetic analysis, such as convergence rates of posterior split probabilities and branch lengths. Graphical exploration of the output from phylogenetic MCMC simulations gives intuitive and often crucial information on the success and reliability of the analysis. The tool presented here complements convergence diagnostics already available in other software packages primarily designed for other applications of MCMC. Importantly, the common practice of using trace-plots of a single parameter or summary statistic, such as the likelihood score of sampled trees, can be misleading for assessing the success of a phylogenetic MCMC simulation. The program is available as source under the GNU General Public License and as a web application at http://ceb.scs.fsu.edu/awty.
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              An algorithm for progressive multiple alignment of sequences with insertions.

              Dynamic programming algorithms guarantee to find the optimal alignment between two sequences. For more than a few sequences, exact algorithms become computationally impractical, and progressive algorithms iterating pairwise alignments are widely used. These heuristic methods have a serious drawback because pairwise algorithms do not differentiate insertions from deletions and end up penalizing single insertion events multiple times. Such an unrealistically high penalty for insertions typically results in overmatching of sequences and an underestimation of the number of insertion events. We describe a modification of the traditional alignment algorithm that can distinguish insertion from deletion and avoid repeated penalization of insertions and illustrate this method with a pair hidden Markov model that uses an evolutionary scoring function. In comparison with a traditional progressive alignment method, our algorithm infers a greater number of insertion events and creates gaps that are phylogenetically consistent but spatially less concentrated. Our results suggest that some insertion/deletion "hot spots" may actually be artifacts of traditional alignment algorithms.
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                Author and article information

                Journal
                101698577
                46074
                Nat Ecol Evol
                Nat Ecol Evol
                Nature ecology & evolution
                2397-334X
                8 February 2019
                18 March 2019
                April 2019
                18 September 2019
                : 3
                : 4
                : 668-678
                Affiliations
                [1 ]Synthetic and Systems Biology Unit, Biological Research Centre, Hungarian Academy of Sciences, H-6726 Szeged, Hungary
                [2 ]Department of Plant Anatomy, Institute of Biology, Eötvös Loránd University, Pázmány Péter sétány 1/C, H-1117 Budapest, Hungary
                [3 ]Clark University, Biology Department, 950 Main street, 01610 Worcester, Ma, USA
                [4 ]Department of Ecology and Evolutionary Biology, University of Toronto, M5S 3B2, Toronto, Ontario, Canada
                [5 ]MTA-ELTE ‘Lendület’ Evolutionary Genomics Research Group, Department of Biological Physics, Eötvös Loránd University, Pázmány Péter sétány 1/A, H-1117 Budapest, Hungary
                [6 ]Department of Microbiology, Faculty of Science and Informatics, University of Szeged, Közép 52, 6726 Szeged, Hungary
                [7 ]Department of Botany, Faculty of Horticultural Science, Szent István University, H-1518 Budapest, Hungary
                [8 ]Hungarian Mycological Society, P.O. Box 89, H-1300 Budapest Hungary
                [9 ]US Department of Energy (DOE) Joint Genome Institute, Walnut Creek, CA, 94598, United States
                [10 ]Via Cappuccini, 78, 33170 Pordenone, Italy
                [11 ]Jardin Botanico Nacional Ma. Moscoso, Santo Domingo, Dominican Republic
                [12 ]Department of Botany, Moravian Museum, Zelný trh 6, 659 37, Brno, Czech Republic
                [13 ]Western Australian Herbarium, Science and Conservation, Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia
                [14 ]Manaaki Whenua – Landcare Research, Private Bag 92170, Auckland 1142, New Zealand
                [15 ]Institut de Systématique, Evolution, Biodiversité (ISYEB - UMR 7205), Muséum National d’Histoire Naturelle, Sorbonne Université, CNRS, CP 39, 12 Rue Buffon, F-75005 Paris, France
                [16 ]State Herbarium of South Australia, G.P.O. Box 1047, Adelaide, South Australia 5001, Australia
                [17 ]Manaaki Whenua – Landcare Research, PO Box 69040, Lincoln 7640, New Zealand
                [18 ]Oberfeldstraße 9, A-5113 St. Georgen bei Salzburg, Austria
                [19 ]Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA, USA
                [20 ]Zsombolyai u. 56., H-8000, Székesfehérvár, Hungary
                [21 ]Naturalis Biodiversity Center, Leiden, the Netherlands
                [22 ]Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, USA
                [23 ]Department of Mycology, W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, Poland
                [24 ]Natural History Museum, Slovak National Museum, Vajanského nábr. 2, SK–810 06 Bratislava, Slovakia
                [25 ]Finnish Environment Institute, Biodiversity Unit, P.O. Box 140, Helsinki, FI-00251 Finland
                [26 ]CONICET - Universidad de Buenos Aires, Instituto de Micología y Botánica (InMiBo), DBBE, FCEN, Ciudad Universitaria Pab. II (1428) Buenos Aires, Argentina
                [27 ]The Jodrell Laboratory, Royal Botanic Gardens, Kew, Surrey TW9 3AB, UK
                [28 ]Damjanich u. 54, H-1071 Budapest Hungary
                [29 ]Department of Biology, Microbiology, Utrecht University, 3584CH Utrecht, The Netherlands
                [30 ]Center for Forest Mycology Research, US-Forest Service, Northern Research Station, Madison, USA
                [31 ]Department of Biology, University of Central Oklahoma, Edmond, OK 73034, USA
                [32 ]Botanical Museum, University of Helsinki, PO Box 7, 00014, Helsinki, Finland
                [33 ]Institute of Plant and Animals Ecology, Russian Academy of Sciences, 8 March str. 202, 620144 Ekaterinburg, Russia
                [34 ]Swedish Museum of Natural History, Department of Cryptogamic Botany, Box 50007, S-104 05 Stockholm, Sweden
                [35 ] Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 3, 613 00, Brno, Czech Republic
                [36 ]Herbarium Rooseveltensis Amanitarum P. O. Box 57, Roosevelt, New Jersey 08555-0057, USA; Res. Assoc. (hons.), the New York Botanical Garden, Bronx, New York
                [37 ]Plant and Microbial Biology, University of California, Berkeley, CA 94703, USA
                [38 ] Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720, United States
                [39 ]Institut National de la Recherche Agronomique (INRA), Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE), UMR 1136, Champenoux, France
                Author notes
                [* ]Correspondence to: lnagy@ 123456fungenomelab.com
                [&]

                Current address: Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia

                [&&]

                Current address: MTA-SZTE ‘Lendulet’ Fungal Pathogenicity Mechanisms Research Group, Kozep fasor 52, 6726 Szeged, Hungary

                [#]

                Current address: Section for Genetics and Evolutionary Biology (EVOGENE), University of Oslo, Blindernveien 31, 0316 Oslo, Norway

                Article
                EMS81575
                10.1038/s41559-019-0834-1
                6443077
                30886374
                f6646901-47bf-4d8d-b415-7061fc9a982a

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