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Unexpected species diversity and contrasting evolutionary hypotheses in Hebeloma (Agaricales) sections Sinapizantia and Velutipes in Europe

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Abstract

Hebeloma velutipes is one of the most common and abundant members of the ectomycorrhizal basidiomycete genus and H. sinapizans is one of its oldest and most commonly recorded species. Using large sample sizes, several loci and the analysis of types, we explored the taxonomy, species limits, distribution and the infrageneric classification of these two species and their relatives. By relying almost exclusively on sequenced material, we were able to attain a marked refinement of species descriptions. Phylogenetic results are congruent with respect to the delimitation of species, but suggest conflicting evolutionary histories of the species phylogeny. Using multi-species coalescent analysis, phylogenetic support for H. sects. Velutipes and Sinapizantia was assessed, finding clear support for H. sect. Sinapizantia but ambiguous results for H. sect. Velutipes. One species, H. subconcolor, previously accommodated in H. sect. Denudata, is placed in H. sect. Velutipes. Hebeloma bulbiferum, so far not considered in systematic treatments, is shown to belong to H. sect. Sinapizantia. Unexpectedly, H. velutipes turned out to be distinct from H. leucosarx. Hebeloma erebium comb. nov., H. celatum sp. nov. and H. quercetorum, formerly treated as a single species (H. quercetorum), are demonstrated to be three taxa that are clearly distinct in molecular terms, even though, morphologically, they can be deceptively similar; H. erebium and H. quercetorum are, moreover, geographically distinct. The morphological characters used to distinguish the ten recognised European species are outlined. Finally, a lectotype and an epitype are designated for H. sinapizans and a lectotype for H. quercetorum.

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Acknowledgments

We are very much obliged to A. Bogaerts from the herbarium in Meise (BR) and G. Lalli (AQUI) for handling loans. Our grateful thanks also go to Th.W. Kuyper for kindly making available to us material used by D.K. Aanen from WBS now L, as well as the curators of the herbaria BR, C, E, G, K, IB, L, LIP, LY, MCVE, MICH, MPU, PC, RO, SOMF, TUR, WU and ZT for the loan of collections for study and sequencing. Furthermore, we very much appreciated the help of A. Andrews, P. Ardron, B. Assyov, I. Assyova, L. Ballester, E. Bizio, J. Borovička, A. Bracke, B. Brand, E. Campo, A. Cappelli, M. Carbone, G. Corriol, P. Cullington, L. Davies, D. Deschuyteneer, E. Egli, F. Draye, A. Gennari, M. Ghyselinck, A. Hausknecht, J. Heilmann-Clausen, A. Henrici, P. Hilb, C. Hobart, S. Huhtinen, L. Jalink, I. Kałucka, M.Karadelev, D. Karansinski, S. Kelly, G. Kibby, D. Laber, C. Lecuru, M. Lenne, B. Levesen, M. Lozides, J.P. Marice, M. Meusers, G. Mir, P.-A. Moreau, S. Poumarat, I. Salcedo, J.C. Schou, S. Pizzardo, S. Skeates, A. Szczepkouski, M. Tassi, A. Taylor, M. Theiss, T. Tokov, M. Tortelli, J. Vauras, J. Volders, R. Watling and J. Weir for supplying us with interesting Hebeloma collections. G. Pacioni of the Department of Life, Health and Environmental Sciences, University of L’Aquila, Italy, is thanked for the use of sequencing facilities. Numerous people have helped in the lab to generate Hebeloma sequence data that were used directly or indirectly in this study. We would like to thank K. Dukik (CBS-KNAW Fungal Biodiversity Centre Utrecht), U. Fürst, S. Garnica and J. Schade (Universität Tübingen), and R. Gadjieva, M. Jonsson, C. Lundström, J. Petterson and D. Öncü (SLU Uppsala), as well as the Uppsala University Genome Center, the Hubrecht Institute sequence facility and LGC. Special thanks go to P.-A. Moreau for suggesting that Naucoria erebia might be a Hebeloma. Finally, we are indebted to Luis Parra Sanchez and David Hawksworth for their invaluable help in solving several knotty nomenclatural problems posed by some of the taxa treated in this study.

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Authors and Affiliations

  1. Via Tiburtina Valeria 55/A, 65026, Popoli, Italy

    Edmondo Grilli

  2. Rue Père de Deken 19, 1040, Brussels, Belgium

    Henry J. Beker

  3. Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    Henry J. Beker

  4. Staatliches Museum für Naturkunde Stuttgart, Rosenstein 1, 70191, Stuttgart, Germany

    Ursula Eberhardt & Nicole Schütz

  5. Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Ursula Eberhardt

  6. Department of Life, Health and Environmental Sciences, University of L’Aquila, Via Vetoio snc - Edificio Coppito I, 67100, Coppito, AQ, Italy

    Marco Leonardi

  7. Department of Life Sciences and Systems Biology, Università degli Studi di Torino, Viale P.A. Mattioli 25, 10125, Turin, Italy

    Alfredo Vizzini

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  1. Edmondo Grilli
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Correspondence to Ursula Eberhardt.

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Grilli, E., Beker, H.J., Eberhardt, U. et al. Unexpected species diversity and contrasting evolutionary hypotheses in Hebeloma (Agaricales) sections Sinapizantia and Velutipes in Europe. Mycol Progress 15, 5 (2016). https://doi.org/10.1007/s11557-015-1148-6

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