Diptera: Ceratopogonidae) Dustin Swanson Clemson University, [email protected]
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Clemson University TigerPrints All Dissertations Dissertations 8-2012 Ecology and Phylogeny of the Biting-Midge Genus Culicoides (Diptera: Ceratopogonidae) Dustin Swanson Clemson University, [email protected] Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations Part of the Entomology Commons Recommended Citation Swanson, Dustin, "Ecology and Phylogeny of the Biting-Midge Genus Culicoides (Diptera: Ceratopogonidae)" (2012). All Dissertations. 1002. https://tigerprints.clemson.edu/all_dissertations/1002 This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. ECOLOGY AND PHYLOGENY OF THE BITING-MIDGE GENUS CULICOIDES (DIPTERA: CERATOPOGONIDAE) A Dissertation Presented to the Graduate School of Clemson University In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Entomology by Dustin A. Swanson August 2012 Accepted by: Dr. Peter H. Adler, Committee Chair Dr. Matthew W. Turnbull Dr. John C. Morse Dr. Bryan L. Brown ABSTRACT Flies of the genus Culicoides are small, biting midges in the family Ceratopogonidae. These flies are of medical, veterinary, and economic importance because their blood-feeding behavior can cause stress to hosts and transmit disease agents. Despite the importance of these flies, little is known about their biology, especially the ecology of the immature stages and the phylogenetic relationships among taxa. The objectives of my study were to address these two areas of Culicoides biology. Larval Culicoides were collected from aquatic habitats in four ecoregions of South Carolina, USA. Eleven ecological variables were recorded for each sample. Larvae were identified by amplifying and sequencing a portion of the COI gene by PCR and performing a BLAST search of an adult COI database. BLAST identifications were confirmed with morphological descriptions. Multiple logistic regression of the ecological variables was conducted on the presence-absence of larval taxa. Eleven species, 1 species complex, and 3 unidentified morphospecies of Culicoides were identified. Logistic regression yielded predictive models for C. furens (Poey), 1853, and C. hollensis (Melander and Brues), 1903 . Culicoides haematopotus Malloch, 1915, was composed of five genetic clusters and two ecological groups, one present in shallow, aquatic habitats associated with hardwood forests and the other with shallow, aquatic habitats in the coast plains ecoregion, indicating a probable species complex. Two larval taxa with distinct morphologies were linked to C. stellifer (Coquillett), 1901, indicating another probable species complex. ii Examination of Culicoides species for potential synapomorphies of the genus yielded two smooth, cuticular structures (scutal areolae) on the scutum just anterior to the scutellum. Scutal areolae were documented in males and females of seven genera of Ceratopogonidae. The scutal areolae were a synapomorphy of the family, with independent losses in the Forcipomyiinae+Dasyheleinae and the Ceratopogonini. In Culicoides and Paradasyhelea, the scutal areolae were modified into raised nodules, supporting a sister group relationship of these taxa. No pores, muscles, or nerves were associated with the scutal areolae, but the structures had light-reflecting properties, indicating a possible role in intraspecific communication. The subgeneric classification of Culicoides was assessed using cladistic analysis. Morphological characters were extracted from the literature and used in a maximum parsimony analysis of the 13 subgenera and 7 species groups of Nearctic Culicoides . Five subgenera and one species group of Culicoides were monophyletic. Three subgenera were polyphyletic and no supporting synapomorphies were found for 10 subgeneric groups. A clade of the subgenera (( Avaritia+Hoffmania )+ Culicoides ) was inferred from the morphological analysis and confirmed by a maximum likelihood analysis of a fragment of the COI gene. Maximum likelihood analysis of an unresolved polytomy, using COI, did not result in improved resolution of the morphological tree, but indicated a species complex for C. stellifer, supporting results from the larval ecology study. iii DEDICATION I dedicate this dissertation to my wife Lane and my son Trent. Thank you for your encouragement, support, and patience while I pursued my dream. iv ACKNOWLEDGEMENTS I have many people to thank for their help making the research and writing that went into this dissertation much easier. First and foremost is my advisor Peter Adler, who expertly guided my curiosity and ambition into a more manageable project and for all of the advice along the way. I also want to thank my other committee members, Matt Turnbull, John Morse, and Bryan Brown, for helping shape my project and for the help whenever I asked. I also want to thank my unofficial committee members Art Borkent and Bill Grogan. My many conversations about Ceratopogonidae with you and your years of expertise were extremely helpful to my research. Ryszard Szadziewski, Gustavo Spinelli, and Peter Cranston were of great help with chapter 4. Matt Lehnert deserves all the credit for the scanning electron micrographs in this dissertation. I would like to give a special thanks to all of those people who helped with securing research sites and permits, Theresa Thom at Congaree National Park, everyone with the South Carolina Department of Parks, Recreation, and Tourism, and Donna Purvis and Merle Sheppard at the Clemson Coastal Research and Education Center. v TABLE OF CONTENTS Page TITLE PAGE .................................................................................................................... i ABSTRACT ..................................................................................................................... ii DEDICATION ................................................................................................................ iv ACKNOWLEDGMENTS ............................................................................................... v LIST OF TABLES ........................................................................................................ viii LIST OF FIGURES ........................................................................................................ ix CHAPTER I. INTRODUCTION AND LITERATURE REVIEW ..................................... 1 Introduction .............................................................................................. 1 Objectives ................................................................................................ 2 Literature Review..................................................................................... 2 Taxonomy ................................................................................................ 2 Phylogeny ................................................................................................ 5 Structure and Function ............................................................................. 7 Ecology .................................................................................................. 21 Medical and Veterinary Importance ...................................................... 24 Studying Culicoides ............................................................................... 26 References .............................................................................................. 29 II. ECOLOGY OF LARVAL CULICOIDES IN SOUTH CAROLINA, USA ................................................................................. 58 Introduction ............................................................................................ 58 Materials and Methods ........................................................................... 59 Results .................................................................................................... 68 Discussion .............................................................................................. 71 References .............................................................................................. 76 vi Table of Contents (Continued) Page III. FUNCTIONAL MORPHOLOGY AND PHYLOGENETIC VALUE OF A SCUTAL STRUCTURE UNIQUE TO THE CERATOPOGONIDAE ...................................................................... 109 Introduction .......................................................................................... 109 Materials and Methods ......................................................................... 111 Results .................................................................................................. 114 Discussion ............................................................................................ 116 References ............................................................................................ 120 IV. PHYLOGENETIC ASSESSMENT OF THE SUBGENERA OF NEARCTIC CULICOIDES ........................................................... 140 Introduction .......................................................................................... 140 Materials and Methods ......................................................................... 141 Results .................................................................................................. 142 Discussion ...........................................................................................