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Studies of the Laboulbeniomycetes: Diversity, Evolution, and Patterns of Speciation

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Studies of the Laboulbeniomycetes: Diversity, Evolution, and Patterns of Speciation Studies of the Laboulbeniomycetes: Diversity, Evolution, and Patterns of Speciation The Harvard community has made this article openly available. Please share how this access benefits you. Your story matters Citable link http://nrs.harvard.edu/urn-3:HUL.InstRepos:40049989 Terms of Use This article was downloaded from Harvard University’s DASH repository, and is made available under the terms and conditions applicable to Other Posted Material, as set forth at http:// nrs.harvard.edu/urn-3:HUL.InstRepos:dash.current.terms-of- use#LAA ! STUDIES OF THE LABOULBENIOMYCETES: DIVERSITY, EVOLUTION, AND PATTERNS OF SPECIATION A dissertation presented by DANNY HAELEWATERS to THE DEPARTMENT OF ORGANISMIC AND EVOLUTIONARY BIOLOGY in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the subject of Biology HARVARD UNIVERSITY Cambridge, Massachusetts April 2018 ! ! © 2018 – Danny Haelewaters All rights reserved. ! ! Dissertation Advisor: Professor Donald H. Pfister Danny Haelewaters STUDIES OF THE LABOULBENIOMYCETES: DIVERSITY, EVOLUTION, AND PATTERNS OF SPECIATION ABSTRACT CHAPTER 1: Laboulbeniales is one of the most morphologically and ecologically distinct orders of Ascomycota. These microscopic fungi are characterized by an ectoparasitic lifestyle on arthropods, determinate growth, lack of asexual state, high species richness and intractability to culture. DNA extraction and PCR amplification have proven difficult for multiple reasons. DNA isolation techniques and commercially available kits are tested enabling efficient and rapid genetic analysis of Laboulbeniales fungi. Success rates for the different techniques on different taxa are presented and discussed in the light of difficulties with micromanipulation, preservation techniques and negative results. CHAPTER 2: The class Laboulbeniomycetes comprises biotrophic parasites associated with arthropods and fungi. Two orders have been recognized, Laboulbeniales and Pyxidiophorales. The phylogenetic reconstruction of a large three-gene dataset reveals a third order, Herpomycetales nom. prov., containing the single genus Herpomyces, which now comprises 26 species. Species of Herpomyces exclusively parasitize cockroaches (Blattodea). A new species, H. shelfordellae nom. prov., is described based on morphology and analysis of the ITS ribosomal DNA. The new rankless taxon ‘Laboulbeniomyceta’ is used for the well-resolved node that describes the most recent common ancestor of Laboulbenionycetes and sister class Sordariomycetes. CHAPTER 3: Using the morphological species concept, Hesperomyces virescens ! iii ! (Laboulbeniales) has been recognized as a single species with an almost global distribution and a host range encompassing 30 ladybird hosts (Coccinellidae). Using sequence data from three gene regions – SSU, ITS and LSU rDNA, evidence is presented for distinct clades within Hesperomyces virescens, each clade restricted to a single host species. Species delimination methods confirm that the lineages within H. virescens sensu lato correspond to species. The combination of morphometric, molecular phylogenetic and ecological data provides support for an integrative taxonomy approach. CHAPTER 4: Arthrorhynchus, Gloeandromyces and Nycteromyces (Laboulbeniales), are ectoparasitic on bat flies (Diptera), which are ectoparasitic on bats (Chiroptera). Sequence data from two genes reveal that parasitism of bat flies by Laboulbeniales independently arose three times. Of seven morphologically distinct taxa of Gloeandromyces, four are delimited as separate species by molecular methods. Gloeandromyces dickii nom. prov. is described and illustrated. Both G. pageanus and G. streblae show divergence correlated with host specialization. Position- induced morphological adaptations are observed and discussed. Parasite-host associations between bat flies and Laboulbeniales are explained by roosting ecology of the bat hosts. CHAPTER 5: Owing to difficulties in DNA extraction and amplification of phylogenetically informative genes, the phylogeny of the class Laboulbeniomycetes has been severely understudied. Here, based on a dataset of 83 small subunit ribosomal DNA sequences, a preliminary class-wide phylogeny is presented. The three orders Herpomycetales, Laboulbeniales and Pyxidiophorales are strongly supported, but several current higher taxa (subtribes, tribes, subfamilies) are polyphyletic. Earliest diverging genera in the Laboulbeniales tree are those that have aquatic hosts. Compound antheridia have arisen multiple times independently. Structurally based classification needs revision. ! iv ! TABLE OF CONTENTS ABSTRACT ................................................................................................................................... iii TABLE OF CONTENTS .................................................................................................................v ACKNOWLEDGEMENTS ........................................................................................................... ix INTRODUCTION TO LABOULBENIALES ................................................................................1 FUNGAL PARASITES .......................................................................................................2 OVERVIEW OF LABOULBENIOMYCETES ..................................................................3 SOME HISTORICAL NOTES ............................................................................................7 A MODEL TO STUDY SYMBIOTIC RELATIONSHIPS ..............................................11 MORPHOLOGY OF LABOULBENIALES .....................................................................13 ASSOCIATIONS WITH THEIR HOSTS .........................................................................19 OBJECTIVES OF THE DISSERTATION .......................................................................27 LITERATURE CITED ......................................................................................................29 CHAPTER 1: Bringing Laboulbeniales into the 21st century: enhanced techniques for extraction and PCR amplification of DNA from minute ectoparasitic fungi .................................................41 Abstract ..............................................................................................................................44 INTRODUCTION .............................................................................................................44 ! v ! MATERIAL AND METHODS .........................................................................................48 RESULTS ..........................................................................................................................53 DISCUSSION ....................................................................................................................56 CONCLUSIONS................................................................................................................62 ACKNOWLEDGEMENTS ...............................................................................................63 LITERATURE CITED ......................................................................................................64 CHAPTER 2: Birth of an order: comprehensive phylogenetic study excludes Herpomyces (Fungi, Laboulbeniomycetes) from Laboulbeniales ......................................................................70 Abstract ..............................................................................................................................72 INTRODUCTION .............................................................................................................73 MATERIAL AND METHODS .........................................................................................76 RESULTS ..........................................................................................................................85 TAXONOMY ....................................................................................................................99 Herpomycetales nom. prov. ...................................................................................99 Herpomyces shelfordellae nom. prov. .................................................................100 DISCUSSION ..................................................................................................................103 ACKNOWLEDGEMENTS .............................................................................................112 LITERATURE CITED ....................................................................................................113 ! vi ! CHAPTER 3: Integrative taxonomy reveals hidden species within Hesperomyces virescens (Fungi, Laboulbeniales), a parasite of ladybirds (Coleoptera, Coccinellidae) ............................120 Abstract ............................................................................................................................121 INTRODUCTION ...........................................................................................................121 MATERIAL AND METHODS .......................................................................................126 RESULTS ........................................................................................................................137 DISCUSSION ..................................................................................................................157 CONCLUSIONS..............................................................................................................168
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