Phylogenetic classification ofCordyceps and the clavicipitaceous fungi STUDIES IN MYCOLOGY 57, 2007 Studies in Mycology The Studies in Mycology is an international journal which publishes systematic monographs of filamentous fungi and yeasts, and in rare occasions the proceedings of special meetings related to all fields of mycology, biotechnology, ecology, molecular biology, pathology and systematics. For instructions for authors see www.cbs.knaw.nl. EXECUTIVE EDITOR Prof. dr Robert A. Samson, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] LAYOUT EDITOR Manon van den Hoeven-Verweij, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] SCIENTIFIC EDITORS Prof. dr Uwe Braun, Martin-Luther-Universität, Institut für Geobotanik und Botanischer Garten,Herbarium, Neuwerk 21, D-06099 Halle, Germany. E-mail: [email protected] Prof. dr Pedro W. Crous, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr Walter Gams, Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. E-mail: [email protected] Prof. dr David M. Geiser, Department of Plant Pathology, 121 Buckhout Laboratory, Pennsylvania State University, University Park, PA, U.S.A. 16802. E-mail: [email protected] Dr Lorelei L. Norvell, Pacific Northwest Mycology Service, 6720 NW Skyline Blvd, Portland, OR, U.S.A. 97229-1309. E-mail: [email protected] Dr Erast Parmasto, Institute of Zoology & Botany, 181 Riia Street, Tartu, Estonia EE-51014. E-mail: [email protected] Prof. dr Alan J.L. Philips, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta de Torre, 2829-516 Caparica, Portugal. E-mail: [email protected] Dr Amy Y. Rossman, Rm 304, Bldg 011A, Systematic Botany & Mycology Laboratory, Beltsville, MD, U.S.A. 20705. E-mail: [email protected] Dr Keith A. Seifert, Research Scientist / Biodiversity (Mycology and Botany), Agriculture & Agri-Food Canada, KW Neatby Bldg, 960 Carling Avenue, Ottawa, ON, Canada K1A OC6. E-mail: [email protected] Prof. dr Jeffrey K. Stone, Department of Botany & Plant Pathology, Cordley 2082, Oregon State University, Corvallis, OR, U.S.A. 97331-2902. E-mail: [email protected] Dr Richard C. Summerbell, 27 Hillcrest Park, Toronto, Ont. M4X 1E8, Canada. E-mail: [email protected] Copyright 2007 Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. All rights reserved. No part of this work covered by the copyright herein may be reproduced or used in any form or by any means - graphic, electronic, or mechanical, including photocopying, recording, taping or information storage and retrieval systems - without permission of the publisher. Publication date: 31 May 2007 Published and distributed by Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. Internet: www.cbs.knaw.nl. E-mail: [email protected]. ISBN/EAN : 978-90-70351-66-3 Online ISSN : 1872-9797 Print ISSN : 0166-0616 Cover: Top: Cordyceps gracilis on lepidopteran larva, EFCC 10121; Beauveria sp. on adult of beetle (Coleoptera), EFCC 1357; Hirsutella sp. on wasp (Hymenoptera); Bottom: C. cardinalis, section of perithecia in stroma, OSC 93609; C.cf. pruinosa on lepidopteran pupa (Limacodidae), EFCC 11756; C. militaris, ascus with disarticulating ascospores, OSC 93623. Phylogenetic classification ofCordyceps and the clavicipitaceous fungi Gi-Ho Sung Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331–2902, U.S.A. Nigel L. Hywel-Jones Mycology Laboratory, National Center for Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand Jae-Mo Sung Department of Applied Biology and Entomopathogenic Fungal Culture Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of Korea J. Jennifer Luangsa-ard Phylogenetics Laboratory, National Center for Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand Bhushan Shrestha Department of Applied Biology and Entomopathogenic Fungal Culture Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of Korea and Joseph W. Spatafora Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331–2902, U.S.A. edited by Walter Gams Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands An institute of the Royal Netherlands Academy of Arts and Sciences CONTENTS EDITORIAL AND REFLECTION ..............................................................................................................................1 Gi-Ho Sung, Nigel L. Hywel-Jones, Jae-Mo Sung, J. Jennifer Luangsa-ard, Bhushan Shrestha and Joseph W. Spatafora: Phylogenetic classification of Cordyceps and the clavicipitaceous fungi INTRODUCTION ...................................................................................................................................................... 6 Materials AND METHODS ..................................................................................................................................8 Results .................................................................................................................................................................9 DISCUSSION ........................................................................................................................................................ 13 Phylogenetic implications on the systematics of the genus Cordyceps ............................................................ 13 Species in Clavicipitaceae clade A ................................................................................................................... 16 Species in Clavicipitaceae clade B ................................................................................................................... 17 Species in Clavicipitaceae clade C ................................................................................................................... 20 The taxonomic utility of anamorphic forms in classification of Cordyceps ....................................................... 22 TAxONOMIC REvISION ....................................................................................................................................... 25 Clavicipitaceae Clade A .................................................................................................................................... 25 Clavicipitaceae .............................................................................................................................................27 Metacordyceps ................................................................................................................................................. 27 Accepted names and new combinations in Metacordyceps ....................................................................35 New combinations for anamorphs associated with Metacordyceps ........................................................35 Clavicipitaceae Clade B .....................................................................................................................................35 Ophiocordycipitaceae ...................................................................................................................................35 Elaphocordyceps ..........................................................................................................................................36 Accepted names and new combinations in Elaphocordyceps ............................................................... 37 Ophiocordyceps .......................................................................................................................................... 38 Accepted names and new combinations in Ophiocordyceps ..................................................................39 Clavicipitaceae Clade C .................................................................................................................................... 48 Cordycipitaceae ........................................................................................................................................... 48 Cordyceps .................................................................................................................................................... 48 Accepted names and new combinations in Cordyceps .......................................................................... 48 Clavicipitaceae incertae sedis .................................................................................................................50 Residual species of Cordyceps ..........................................................................................................50 KEY to THE GENERA OF FUNGI formerly CLASSIFIED IN CORDYCEPS ................................................54 ACKNOWLEDGEMENTS ......................................................................................................................................56 REFERENCES ........................................................................................................................................................56 INDEx OF FUNGAL NAMES ..................................................................................................................................60