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Exploring Species Boundaries in the Diatom Genus Rhoicosphenia Using Morphology, Phylogeny, Ecology, and Biogeography Evan William Thomas

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Exploring Species Boundaries in the Diatom Genus Rhoicosphenia Using Morphology, Phylogeny, Ecology, and Biogeography Evan William Thomas University of Colorado, Boulder CU Scholar Ecology & Evolutionary Biology Graduate Theses & Ecology & Evolutionary Biology Dissertations Spring 1-1-2016 Exploring Species Boundaries in the Diatom Genus Rhoicosphenia Using Morphology, Phylogeny, Ecology, and Biogeography Evan William Thomas Follow this and additional works at: http://scholar.colorado.edu/ebio_gradetds Part of the Ecology and Evolutionary Biology Commons, Environmental Microbiology and Microbial Ecology Commons, Molecular Biology Commons, and the Systems Biology Commons This Dissertation is brought to you for free and open access by Ecology & Evolutionary Biology at CU Scholar. It has been accepted for inclusion in Ecology & Evolutionary Biology Graduate Theses & Dissertations by an authorized administrator of CU Scholar. For more information, please contact [email protected]. i EXPLORING SPECIES BOUNDARIES IN THE DIATOM GENUS RHOICOSPHENIA USING MORPHOLOGY, PHYLOGENY, ECOLOGY, AND BIOGEOGRAPHY by EVAN WILLIAM THOMAS B.A., University of Michigan, 2005 M.S., Bowling Green State University, 2007 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2016 ii This thesis entitled: Exploring species boundaries in the diatom genus Rhoicosphenia using morphology, phylogeny, ecology, and biogeography written by Evan William Thomas has been approved for the Department of Ecology and Evolutionary Biology ––––––––––––––––––––––––––––––––––– Dr. Andrew P. Martin ––––––––––––––––––––––––––––––––––– Dr. Steven K. Schmidt Date____________ The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. iii Abstract Thomas, Evan William (Ph.D., Ecology and Evolutionary Biology) Exploring species boundaries in the diatom genus Rhoicosphenia using morphology, phylogeny, ecology, and biogeography Thesis directed by Professor Andrew P. Martin Certain taxonomic groups within the American flora and fauna are relatively unexplored in terms of their biodiversity – one of these groups are the diatoms. The diversity, phylogeny, and ecology of the common freshwater diatom genus Rhoicosphenia are explored. While determining the diversity of Rhoicosphenia in American streams, several new taxa have been discovered, both from fossil and recent collections. These discoveries are discussed in the context of the history of the genus, its diversity in other parts of the world, and the morphological characters used to identify species distinctions. Prior to this dissertation, one taxon (R. abbreviata) was commonly reported from the United States, and after these studies, eight morphologically distinct taxa were found. Presently, no published molecular studies have sequenced any species of Rhoicosphenia for use in phylogenetic analyses. In the literature, four historical hypotheses (dating back to the erection of the genus in 1860) about its position in the diatom tree of life remain untested by molecular data. This dissertation used morphological and multi-marker molecular data to test the four hypotheses and place Rhoicosphenia in the phylogeny of diatoms. The results did not fully support any of the four hypotheses, but did offer insight into parts of the diatom tree that have been underexplored. R. abbreviata was reported from nearly all floristic treatments of diatoms of the US, but little quantitative data was provided in regards to its niche. Due to its presence in a large percentage of studies, it has often been iv referred to as a geographically cosmopolitan species with broad tolerance of ecological parameters. Large water quality monitoring datasets were analyzed to understand the biogeographical patterns of the eight new taxa as well as their ecological niches. Results suggest that none of the taxa are cosmopolitan and none are broadly tolerant of all ecological conditions, but there is variation in both range size and ecological tolerance among the eight taxa. Traditionally, diatom species have been described based largely on morphological variation of their silica cell walls, but the results of the many aspects of this dissertation provide evidence for a more robust, unified species concept for diatoms that relies on many different types of data in addition to morphology, including geographical distributions, ecological preferences, and phylogenetics. v Dedication – This dissertation is dedicated to my children: Alexander, Julian, and Everett. You can do anything you want in life, as long as you ensure that you are kind to all you meet. vi Acknowledgments – During the time working on my dissertation I have encountered many people who are exceedingly deserving of thanks, which I will attempt to provide in this section. My wife, Jennifer Ress, who has been by my side before I started my dissertation and is by my side today – your encouragement and assistance in all aspects of our lives helped make this dissertation possible – I love you. My boys, Alexander, Julian, and Everett, you are all so special to me! No matter how long or short of a day I spent working on my dissertation or teaching, you were always ready to play when Daddy came home. Let’s play some more now that this is all done! To my parents, siblings, grandparents, and friends – you always let me tell you about my dissertation and were usually slightly interested, thank you. Dr. Andy Martin – you allowed me to use my creativity to pursue my interests and I am very grateful for the time we worked together. To my committee members, Dr. Steve Schmidt, Dr. Sam Flaxman, Dr. Nancy Emery, and Dr. Steve Lamos, I greatly appreciate your time and advice. To my many research mentors, past and present, thank you for imparting upon me the skills to observe my surroundings, ask questions, and plan projects to study the unstudied. To Dr. Patrick Kociolek, who provided many opportunities for me to pursue my passion and guided me through many years of my PhD. I am grateful for the Jessup Award allowing me access to Rhoicosphenia across the US while at the Diatom Herbarium of the Academy of Natural Sciences in Philadelphia, with special thanks to Dr. Marina Potapova for her support and encouragement. To the EBIO department at CU, which is full of amazing people – faculty, graduate and undergraduate students, and staff, many of whom directly or indirectly helped me realize my goal of finishing my dissertation – thank you all so much. Finally, to all those not mentioned directly, thank you! vii CONTENTS CHAPTER I. INTRODUCTION ....................................................................................1 Summary remarks ...............................................................................6 II. HISTORY AND TAXONOMY OF RHOICOSPHENIA .........................8 Introduction and taxonomic history ....................................................8 Current understanding of Rhoicosphenia diversity in the US ..........10 Thomas & Kociolek 2015 .................................................................11 Thomas, Kociolek & Karthick 2015 .................................................54 Note on published manuscripts .........................................................85 Descriptions of new morphospecies from the US.............................86 Concluding remarks ..........................................................................96 III. POSITION OF RHOICOSPHENIA IN DIATOM PHYLOGENY ........97 IV. MONOPHYLY OF THE RHOICOSPHENIACEAE ..........................139 Introduction .....................................................................................139 Majewska, Kociolek, Thomas, et al. 2015 ......................................141 V. EXPLORING RHOICOSPHENIA SPECIES BOUNDARIES ............162 REFERENCES….………………………..…………………………………………202 APPENDIX A. Samples examined for ecological analyses ...........................................221 viii TABLES CHAPTER II 1. Ecological data for observed distributions of new Rhoicosphenia............... 15 2. Type locations for new species from California ...........................................15 3. Taxon comparison and trait summary of California taxa .......................17–18 4. Type locations for new fossil species ...........................................................57 5. Taxon comparison and trait summary of fossil taxa .....................................78 6. List of diatom genera found in samples with fossil taxa ..............................80 CHAPTER III 1. Sampling locations for sequenced Rhoicosphenia populations ..................106 2. GenBank accession numbers for sequenced Rhoicosphenia populations...107 3. GenBank accession numbers for other sequences used in analyses ...107–111 4. Primers used in amplification and sequencing of SSU, LSU, and rbcL….112 5. Characters and character states used in morphological analysis ........117–119 6. Taxon and character matrix used in morphological analysis ..............120–122 7. Summary of Hypothesis Testing Results ....................................................127 CHAPTER IV 1. Characters and character states used in morphological analysis ........147–148 2. Taxon and character matrix used in morphological analysis ..............149–150 CHAPTER V 1. Comparison of species based on morphology ............................................170 2. Percentage of sites shared by species pairs
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