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EVOLUTION and DEVELOPMENT of a NOVEL TRAIT in SEPSIDAE a Dissertation Submitted to the Graduate Faculty of the North Dakota Stat

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EVOLUTION and DEVELOPMENT of a NOVEL TRAIT in SEPSIDAE a Dissertation Submitted to the Graduate Faculty of the North Dakota Stat EVOLUTION AND DEVELOPMENT OF A NOVEL TRAIT IN SEPSIDAE A Dissertation Submitted to the Graduate Faculty of the North Dakota State University of Agriculture and Applied Science By Dacotah Michael Melicher In Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY Major Department: Biological Sciences March 2016 Fargo, North Dakota North Dakota State University Graduate School Title EVOLUTION AND DEVELOPMENT OF A NOVEL TRAIT IN SEPSIDAE By Dacotah Michael Melicher The Supervisory Committee certifies that this disquisition complies with North Dakota State University’s regulations and meets the accepted standards for the degree of DOCTOR OF PHILOSOPHY SUPERVISORY COMMITTEE: Dr. Julia Bowsher Chair Dr. Steve Travers Dr. Kendra Greenlee Dr. Philip McClean Approved: 3/23/16 Dr. Wendy Reed Date Department Chair ABSTRACT Evolutionary novelty, the appearance of new traits with no existing homology, is central to the adaptive radiation of new species. Novel traits inform our understanding of development and how developmental mechanisms can generate novelties. Sepsid flies (Diptera: Sepsidae) have a sexually dimorphic, jointed appendage used for courtship and mating. The appendage develops from the fourth abdominal histoblast nest rather than an imaginal disc. Histoblast nests in other species produce the adult epidermis and lack three-dimensional organization. The sepsid system is an opportunity to investigate the evolutionary history of a novel trait and the developmental mechanisms that pattern epidermal tissue into a complex structure. The appendage has a complex history of gain, loss, and recovery over evolutionary time. Appendage morphology is highly variable between species and does not correlate to body size. I collected larval epidermal tissue from 16 species across Sepsidae and one outgroup to trace the evolutionary history of gain, secondary loss, and recovery. I characterized histoblast nests in all segments and sexes, determining the nest size, number, and size of cells. The appendage- producing nest is sexually dimorphic in species after primary gain. Loss of the appendage shows a return to ancestral state while regain shows an increase in nest size in both sexes. The loss of sex dimorphism may indicate that mechanisms involved in specification may be active in females while genes involved in patterning are not activated during pupation. I assembled and annotated a reference transcriptome for the sepsid Themira biloba at using a custom bioinformatic pipeline that uses a merged assembly approach to maximize quality. This pipeline demonstrated an improvement over other methodologies using multiple published metrics for determining quality and completion. This pipeline also demonstrates how cloud computing architecture can complete bioinformatic tasks quickly and at low cost. iii I used the T. biloba transcriptome to identify differentially expressed genes involved in appendage patterning during pupation. I sequenced the appendage producing fourth male larval segment and the third male and fourth female segments. Many of the differentially expressed transcripts are involved in cell signaling, epidermal growth, and transcripts involved morphological development in other species. iv ACKNOWLEDGEMENTS I would like to thank my advisor, Dr. Julia Bowsher, for accepting me as her first doctoral graduate student. Over the term of my graduate career she has given me invaluable mentoring and advice while exhibiting great patience and optimism. I would like to thank my committee members, Dr. Kendra Greenlee, Dr. Steven Travers, and Dr. Phil McClean for their guidance and review of my work. I thank Dr. Wendy Reed for introducing me to my advisor and providing me with guidance entering the graduate program and for her continued advice and support. The NDSU Department of Biological Sciences as a whole has provided me with a comfortable and friendly research environment, financial support for research and conferences, a social community, and has been a second home to me during my undergraduate and graduate academic career. I thank members of the Bowsher lab for their continued support and friendship; Bodini Herath, Alex Torson, Garett Slater, and Bryan Helm. Many collaborators assisted in the production of the research presented in this dissertation. I thank Dr. Ian Dworkin of Michigan State University for hosting myself and Alex Torson during a bioinformatic research exchange and assisting with the construction and review of our bioinformatic pipeline published in 2014. Thanks to Dr. Rudolf Meier of the National University of Singapore for hosting me during my data collection in 2012 and for his continued support with ongoing collaborative projects. Raphael Royette provided invaluable statistical help during data analysis. Pawel Borowicz of the NDSU Advanced Imaging and Microscopy core lab improved the sophistication of our imaging protocols and helped streamline our data collection. I thank George Yocum, Joe Reinhardt, and William Kemp from the Fargo, ND United States Department of Agriculture Agricultural Research Service (USDA ARS) for advice and guidance and internal review of my work as well as an introduction to collaborators. v Thanks to the Evo-Devo-Eco Network (EDEN) for providing travel funding for a research exchange to the Dworkin lab at Michigan State. The National Science Foundation East Asia and Pacific Summer Institute (EAPSI) fellowship allowed me to travel to the Meier lab in Singapore to collect materials and data presented in this dissertation as well as reinforce our collaborative relationship with another member of the sepsid research community. The NDSU Department of Biological Sciences provided startup funding which was used to fund the research presented here as well as a research assistantship and travel funds to attend conferences. The College of Science and Math also provided travel funds and facilitated the work presented here. The USDA ARS also provided financial support in the form of a research assistantship which was vital to the timely completion of my research. I would like to thank Lauren Dennhardt who I met at the beginning of my graduate program and married. She has been my best friend and biggest supporter and convincing her to become my wife is arguably my greatest achievement during my graduate career. Thanks to my parents, Kathleen and Will Cooper, Steve and Cindy Melicher, my siblings, Mary Seelye, Jake, and Anna Melicher, for everything they have done for me over the years that prepared me for my academic and life achievements and being present during these milestones. vi DEDICATION This dissertation is dedicated to my wife Lauren, Kathleen and Will Cooper, Steve and Cindy Melicher, and several thousand sepsid flies, particularly Themira biloba. vii TABLE OF CONTENTS ABSTRACT ................................................................................................................................... iii ACKNOWLEDGEMENTS ............................................................................................................ v DEDICATION .............................................................................................................................. vii LIST OF TABLES ......................................................................................................................... xi LIST OF FIGURES ...................................................................................................................... xii LIST OF ABBREVIATIONS ....................................................................................................... xv LIST OF APPENDIX TABLES .................................................................................................. xvi LIST OF APPENDIX FIGURES................................................................................................ xvii CHAPTER ONE: INTRODUCTION ............................................................................................. 1 An introduction to evolutionary novelty ......................................................................................1 Sepsid novel abdominal appendages ............................................................................................4 Objectives .....................................................................................................................................7 Objective 1: Characterize histoblast nest morphology across Sepsidae ................................. 8 Objective 2: Sequence mRNA from Themira biloba, assemble, and annotate a reference transcriptome........................................................................................................................... 8 Objective 3: Identify transcripts in specific tissues that are involved in appendage development ............................................................................................................................ 9 CHAPTER TWO: SEPSID HISTOBLAST NEST MORPHOLOGY ......................................... 10 Abstract ......................................................................................................................................10 Introduction ................................................................................................................................10 Results ........................................................................................................................................15 Discussion ..................................................................................................................................26
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