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Systematics and Phylogeny of Cordyceps and the Clavicipitaceae with Emphasis on the Evolution of Host Affiliation

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Systematics and Phylogeny of Cordyceps and the Clavicipitaceae with Emphasis on the Evolution of Host Affiliation AN ABSTRACT OF THE DISSERTATION OF Gi-Ho Sung for the degree of Doctor of Philosophy in Botany and Plant Pathology presented on December 1. 2005. Title: Systematics and Phylogeny of Cordyceps and the Clavicipitaceae with Emphasis on the Evolution of Host Affiliation Abstract approved: Redacted for Privacy Cordyceps is a genus of perithecial ascomycetes. It includes over 400 species that are pathogens of arthropods and parasites of the truffle genus Elaphomyces. Based on the morphology of cylindrical asci, thickened ascusapices and fihiform ascospores, it is classified in the Clavicipitaceae (Hypocreales), which also includes endophytes and epiphytes of the grass family (e.g., Claviceps and Epichloe). Multi-gene phylogenetic analyses rejected the monophyly of the Clavicipitaceae. Clavicipitaceous fungi formed three strongly supported clades of which one was monophyletic with the Hypocreaceae. Furthermore, the monophyly of Cordyceps was also rejected as all three clades of Clavicipitaceae included species of the genus. These results did not support the utility of most of the characters (e.g., ascospore morphology and host affiliation) used in current classifications and warranted significant taxonomic revisions of both Cordyceps and the Clavicipitaceae. Therefore, taxonomic revisions were made to more accurately reflect phylogenetic relationships. One new family Ophiocordycipitaceae was proposed and two families (Clavicipitaceae and Cordycipitaceae) were emended for the three clavicipitaceous clades. Species of Cordyceps were reclassified into Cordyceps sensu stricto, Elaphocordyceps gen. nov., Metacordyceps gen. nov., and Ophiocordyceps and a total of 147 new combinations were proposed. In teleomorph-anamorph connection, the phylogeny of the Clavicipitaceae s. 1. was also useful in characterizing the polyphyly of Verticillium sect. Prostrata and in integrating the following major anamorphic genera with their teleomorphic genera in a new classification system(teleomorphic genera: anamorphic genera): Cordyceps: Beauveria,Lecanicillium, Isaria; Hypocrella: Aschersonia; Metacordyceps: Metarhizium, Pochonia; Ophiocordyceps: Hirsutella, Hymenostilbe. In addition to multi-gene phylogenetic analyses, phylogenetic dating and ancestral host state reconstruction were conducted to understand the evolution of host affiliation in Clavicipitaceae s. 1. and the Hypocreales. These analyses suggested that fungal-animal symbioses of the Clavicipitaceae s. 1. initiated in the Jurassic by a series of inter-kingdom host jumps from plant-based nutrition to animal pathogens. A total of 9-14 inter-kingdom host jumps were hypothesized for the Clavicipitaceae s. 1., including 5-7 onto fungi, 2-4 onto animals, and 2-3 onto plants, with dominant ecology as pathogens of arthropods. The total evidence of the Cretaceous radiation of the Clavicipitaceae s. 1. indicated that the current diversity of its fungal-arthropod symbioses may be correlated with the coevolutionary interactions between arthropods and angiosperms in the Cretaceous. ©Copyright by Gi-Ho Sung December 1, 2005 All Rights Reserved Systematics and Phylogeny ofCordycepsand the Clavicipitaceae with Emphasis on the Evolution of Host Affiliation by Gi-Ho Sung A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirement for the degree of Doctor of Philosophy Presented December 1, 2005 Commencement June 2006 Doctor of Philosophy dissertation of Gi-Ho Sung presented on December 1. 2005. APPROVED: Redacted for Privacy Major Professor, representing Botany and Plant Pathology Redacted for Privacy Chair of the Depaltment ofl3otany and Plant Pathology Redacted for Privacy Dean of th4Iiraduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Redacted for privacy Gi-Ho Sung, Author CONTRIBUTION OF AUTHORS Dr. Joseph W. Spatafora was involved in the initiation, design, phylogenetic analyses, and the writing and editing of each manuscript. Drs. Rasoul Zare, Kathie T. Hodge, and Walter Gams were involved in the design and editing of chapter two. Drs. Nigel L. Hywel-Jones and Jae-Mo Sung were not only taxonomic consultants but also contributed to chapter five in providing valuable cultures and specimens. Dr. George 0. Poinar, Jr. was involved in the design and intellectual development of chapter six. TABLE OF CONTENTS Chapter 1: INTRODUCTION .................................................................. 1 Taxonomy and classification ........................................................ 3 Dissertation scope......................................................................6 References ............................................................................... 8 Chapter 2: A REVISION OFVERTICILLIUMSECT.PROSTRATA. II. PHYLOGENETIC ANALYSIS OF SSU AND LSU NUCLEAR rDNA SEQUENCES FROM ANAMORPHS AND TELEOMORPHS OF THE CLAVICIPITACEAE...............................................................13 Abstract ................................................................................ 14 Introduction..............................................................................16 Materials and methods..................................................................19 Taxon sampling..............................................................19 DNA extraction..............................................................20 Phylogenetic analyses......................................................24 Results..............................................................................26 Discussion............................................................................29 Familial relationships of Verticillium sect. Prostrata .................. 29 Polyphyly of Verticillium sect. Prostrata...............................32 Relationships of V. sect. Prostrata with anamorphs and teleomorphs of the Clavicipitaceae.......................................................34 Evolution of host association..............................................37 TABLE OF CONTENTS (Continued) Conclusions ........................................................................... 39 Acknowlegements...................................................................40 References............................................................................40 Chapter 3:CORD YCEPS CARDINALIS SP. NOV.,A NEW SPECIES OF CORD YCEPSWITH AN EAST ASIAN-EASTERN NORTH AMERICAN DISTRIBUTION.....................................................................45 Abstract...............................................................................46 Introduction..............................................................................47 Materials and methods..................................................................49 Field collection...............................................................49 Morphological observations...............................................50 Phylo genetic analyses......................................................51 Taxonomy....................................................................53 Results.................................................................................57 DNAsequencing............................................................57 Phylogenetic analyses......................................................58 Discussion............................................................................60 Morphological comparison of C.cardinaliswith other C. militaris-like species....................................................60 Anamorphic and cultural differences among C.cardinalis,C. militaris and C. pseudomilitaris.....................................................62 TABLE OF CONTENTS (Continued) Phylogenetics of C. cardinalis ............................................. 64 Biogeography of C. cardinalis ............................................. 66 Conclusions ......................................................................... 67 Acknowledgements ................................................................ 68 References ............................................................................ 68 Chapter 4: A MOLECULAR PHYLOGENETIC STUDY OF THE CLAVICIPITACEAE BASED ON MUTIPLE INDEPENDENT LOCI. ..71 Abstract ............................................................................... 72 Introduction..............................................................................74 Materialsand methods..................................................................77 Selection of taxa............................................................78 DNA isolation, PCR amplification, Cloning and Sequencing......78 Phylogenetic analyses......................................................85 Results.................................................................................91 Characteristics of each gene................................................91 Separate analyses and test of incongruence..............................95 The Phylogenetic analyses of the combined data set...................96 Combinational analyses.................................................103 Contribution of each gene partition to nodal support..................105 Discussion......................................................................109 ILD test and the heterogeneity among gene partitions..............109 TABLE OF CONTENTS (Continued) Comparison of phylogenetic methods in
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