University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 12-2015 Systematics and diversification patterns of morphologically and ecologically diverse lineages of Agaricomycetes: Clavariaceae and Cantharellales Joshua Mark Birkebak University of Tennessee - Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Biology Commons, and the Evolution Commons Recommended Citation Birkebak, Joshua Mark, "Systematics and diversification patterns of morphologically and ecologically diverse lineages of Agaricomycetes: Clavariaceae and Cantharellales. " PhD diss., University of Tennessee, 2015. https://trace.tennessee.edu/utk_graddiss/3542 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Joshua Mark Birkebak entitled "Systematics and diversification patterns of morphologically and ecologically diverse lineages of Agaricomycetes: Clavariaceae and Cantharellales." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the requirements for the degree of Doctor of Philosophy, with a major in Ecology and Evolutionary Biology. Patrick B Matheny, Major Professor We have read this dissertation and recommend its acceptance: Randall L. Small, Ernst C. Bernard, Joseph H. Williams Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Systematics and diversification patterns of morphologically and ecologically diverse lineages of Agaricomycetes: Clavariaceae and Cantharellales A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Joshua Mark Birkebak December 2015 Copyright © 2015 by Joshua Mark Birkebak All rights reserved. ii DEDICATION I would like to dedicate this work to my parents Doug and Tambra Birkebak, the best research assistants I have ever had. While some parents may try to dissuade their 12 year old from pursuing mycological endeavors, they not only tolerated it but sacrificed so much time and energy encouraging my fascination. Without their support I never would have made it this far. iii ACKNOWLEDGEMENTS First and foremost I would like to thank my advisor Dr. P. Brandon Matheny who introduced me to the world of scientific side of mycology back in the early 2000’s. He has been a mentor, teacher, and encourager. I would also like to thank my lab mates who have kept me sane (and occasionally driven me insane): Dr. Martin Ryberg, Marisol Sánchez-García, Brian Looney, Emma Harrower, and Hailee Korotkin. Dr. Slavomír Adamčík provided invaluable help and support for Chapter 2 and I am honored to call him a colleague and friend. I would also like to thank my committee: Dr. Randall Small, Dr. Joseph Williams, and Dr. Ernest Bernard. I would like to acknowledge the following societies for their support and opportunities for research and collaboration: Puget Sound Mycological Society, North American Mycological Association, Northeastern Mycological Federation, Mushroom Club of Georgia, and the Mycological Society of America. There are innumerable professional and amateur mycologist that I would like to thank for their support, help with fieldwork, teaching, training, enlightening conversation, and relaxation and they include: Dr. Else Vellinga, Dr. Steve Trudell, Mike Wood, and Jay Justice (the Smokies crew), Dr. Ron Petersen and Dr. Karen Hughes for access to specimens, unpublished notes, literature resources, personal knowledge and general encouragement (The Mycology power couple), Alissa Allen, Christian Schwarz, and Noah Siegel (the Mycohobos), Dr. Jennifer Krauel, Dr. Joe Hughes, and Dr. Doug Kaylor for their years of stimulating conversation at dinners where I learned as much as my years of classwork, and Marian Maxwell (who originally introduced me to mycology) and everyone else at PSMS who supported me from day one. I owe a huge thank you to John Keck for continually being supportive and encouraging. iv ABSTRACT The recent advent of molecular tools and methods to understand the diversity of living organisms allows for exploration of former untestable theories concerning the diversity of fungi. Here we assess the morphologically based classification of the family Clavariaceae in light of molecular phylogenetic reconstruction and propose a revised classification based on natural assemblages. We used stable isotope ratios to uncover a biotrophic nutritional mode for much of the family, which had not been well understood previously. Several enigmatic lineages of agaricoid and cantharelloid fungi within a clade of otherwise clavarioid fruiting bodies are also investigated. The first (partial) support for the Corner hypothesis of morphological evolution is provided. Up to three independent transitions to agaricoid clades and one transition to a cantharelloid clade were uncovered. A new generic classification for agaricoid clades including the discovery of a new genus and species is presented. Finally the effects of morphology and ecology on diversification rates are examined to explore which traits drive patterns of diversity found in the Agaricomycetes. Bayesian Analysis of Macroevolutionary Mixtures (BAMM) and State Speciation and Extinction (BiSSE and MuSSE) analyses were performed on time-calibrated phylogenies of two morphologically and ecologically diverse lineages (the Clavariaceae and the Cantharellales) to test hypotheses that changes in nutritional mode, fruiting body morphology, and hymenophore are associated with shifts in diversification rate. We find that a biotrophic nutritional mode is consistently associated with increased diversification rates while fruiting body morphology and hymenophore are only associated with shifts in the Cantharellales. v TABLE OF CONTENTS INTRODUCTION .................................................................................................. 1 CHAPTER I A systematic, morphological and ecological ..................................... 2 overview of the Clavariaceae (Agaricales) ............................................................ 2 Abstract ............................................................................................................... 3 Introduction .......................................................................................................... 4 Materials and Methods ........................................................................................ 5 Taxon sampling ............................................................................................. 7 DNA extractions, PCR and sequencing ......................................................... 7 Phylogenetic analyses ................................................................................... 8 Ancestral state reconstruction (ASR) analyses .............................................. 8 Stable isotope analysis .................................................................................. 9 Results ................................................................................................................ 9 Ancestral state reconstruction (ASR) analyses ............................................ 13 Stable isotopes ............................................................................................ 14 Discussion ......................................................................................................... 15 Familial compositions .................................................................................. 14 Phylogenetic relationships ........................................................................... 16 Saprotrophic and biotrophic nutritional modes in the Clavariaceae ............. 19 Analysis of GenBank environment sequences............................................. 21 Literature Cited .................................................................................................. 22 Appendix ........................................................................................................... 28 CHAPTER II Testing the Corner hypothesis of fruiting body evolution in the family Clavariaceae (Agaricales) ................................................................................... 47 Abstract ............................................................................................................. 48 Introduction ........................................................................................................ 48 Materials and Methods ...................................................................................... 51 Taxon sampling ........................................................................................... 51 DNA extraction, PCR, and Sequencing ....................................................... 51 Phylogenetic analysis .................................................................................. 52 Divergence time estimation in BEAST ......................................................... 52 BAMM and BiSSE model testing ................................................................