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Evolution and Phylogeny of Basal Winged Insects With EVOLUTION AND PHYLOGENY OF BASAL WINGED INSECTS WITH EMPHASIS ON MAYFLIES (EPHEMEROPTERA) By T. Heath Ogden A dissertation submitted to the faculty of Brigham Young University In partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Integrative Biology Brigham Young University December 2004 BRIGHAM YOUNG UNIVERSITY GRADUATE COMMITTEE APPROVAL of dissertation submitted by T. Heath Ogden This dissertation has been read by each member of the following graduate committee and by majority vote has been found to be satisfactory. __________________________ ________________________________________ Date Michael F. Whiting, Chair __________________________ ________________________________________ Date Keith A. Crandall __________________________ ________________________________________ Date Jack W. Sites __________________________ ________________________________________ Date Richard W. Baumann __________________________ ________________________________________ Date Michel Sartori BRIGHAM YOUNG UNIVERSITY As chair of the candidate’s graduate committee, I have read the dissertation of T. Heath Ogden in its final form and have found that (1) its format, citations, and bibliographical style are consistent and acceptable and fulfill university and department style requirements; (2) its illustrative materials including figures, tables, and charts are in place; and (3) the final manuscript is satisfactory to the graduate committee and is ready for submission to the university library. __________________________ ________________________________________ Date Michael F. Whiting Chair, Graduate Committee Accepted for the Department ________________________________________ Mark C. Belk Graduate Coordinator Accepted for the College ________________________________________ R. Kent Crookston Dean, College of Biology and Agriculture ABSTRACT EVOLUTION AND PHYLOGENY OF BASAL WINGED INSECTS WITH EMPHASIS ON MAYFLIES (EPHEMEROPTERA) T. Heath Ogden Department of Integrative Biology Doctor of Philosophy Ephemeroptera (mayflies) is a monophyletic group of semi-aquatic pterygote insects, comprising 3083 species, 376 genera, and 37 described families and are present on all continents, excluding Antarctica, being associated with freshwater and brackish water habitats. The order is unique among pterygote insects in possessing functional wings at the penultimate molt (subimago stage), prior to the full development of genitalia; in all other insects the presence of functional wings occurs only after the final molt. The purpose of this dissertation is to use molecular and morphological data, in order to investigate the position of the order Ephemeroptera among other insect orders, the higher-level relationships among the major lineages of mayflies, and a detailed analysis of the family Ephemerellidae. Ephemeroptera has been considered by many to be sister to Odonata + Neoptera although alternate hypotheses have been suggested. Data from three molecular loci ambiguously resolve basal pterygote relationships, however, total evidence analysis (combined molecular and morphological data) strongly supports the position of mayflies as sister to all other extant pterygotes. These results and methodologies were recently criticized, and, therefore, the response to the author is included following the manuscript. The phylogenetic relationships among mayfly families is debatable and in some groups unknown. Prior studies have produced phylogenies based on morphological characters mixed with intuition. The first molecular phylogeny for the Order Ephemeroptera is presented. The analyses include 31 of the 37 families, representing ~24% of the genera. The suborders Furcatergalia and Carapacea are supported as monophyletic while Setisura and Pisciforma are not supported as monophyletic. The evolution of the wings, mandibular tusks, burrowing lifestyle, and fishlike body are investigated. Topological sensitivity analysis is used as a tool to examine patterns concerning the stability of relationships across a parameter landscape, providing additional information that may not have been acquired otherwise. The Pannote family Ephemerellidae is comprised of 16 genera and over 300 species and is distinguished from other mayfly families by the absence of the second pair of abdominal gills. The position of Ephemerellidae relative to other closely related pannote mayflies is unclear as are the relationships of the genera within the family. The combined molecular and morphological analyses resulted in a monophyletic Ephemerellidae as sister to the other ephemerelloid families. The subfamily Ephemerellidae was supported as monophyletic, while Timpanoginae had conflicting results. ACKNOWLEDGMENTS I would first like to thank the members of my committee for all the time, assistance, guidance, and patience that they have offered me during my graduate career. They have been valuable in discussions to improve manuscripts and have shaped the way I approach science. I would like to particularly thank Mike Whiting, who as my committee chair has offered me innumerable experiences in the field, in the laboratory, and in the classroom (both as a teacher and a student). He has mentored me in such a way that I am a better researcher, grant writer, teacher, presenter, and colleague. And he has been a support through friendship and example for me and my family. Keith Crandall, has been important as a graduate coordinator and lending important insights to issues, both theoretical and practical, during my time at BYU. Michel, Sartori, has been an important part of the identifying and taxon acquisition of the mayfly specimens. His expertise in mayfly systematics has been much appreciated during the manuscript revision process. It is important to recognize the funding agencies and other resources that have made possible my research. This dissertation was funded by The National Science Foundation Doctoral Dissertation Improvement Grant (DEB-0206505) and a Brigham Young University graduate Fellowship. I should also thank the Department of Integrative Biology (including the Booth Scholarship) and the BYU Office of Graduate Studies for funding for travel to scientific meetings, where results were presented. Finally, I thank the Whiting Laboratory, Department of Integrative Biology, and BYU DNA Sequencing Center for funding and excellent laboratory facilities. Lastly and most importantly, I would like to thank my family for their continued love, patience, and support throughout the last four years. Jimena, my wonderful wife, and Amber and Melissa have made many sacrifices allowing me to go on collecting trips, attend meetings, and spend extra time in the lab in order to permit the completion of my research. I express my love and admiration to Jimena and my girls for this. And I finally express thanks to God for granting me my life, my family, intelligence, and this wonderful world full of his marvelous creations. TABLE OF CONTENTS Title Page…………………………………………………………………………………i Graduate Committee Approval………………………………………………………….ii Final Reading Approval and Acceptance………………………………………….……iii Abstract…………………………………………………………………………….…….iv Acknowledgments…………………………………………………....………………….vi Table of Contents…………………………………………….……..………………….viii Chapter 1: The Problem with “the Paleoptera Problem”: Sense and Sensitivity…………1 Introduction……………………………………………………………………….1 Material and Methods…………………………………………………………….2 Results…………………………………………………………………………….7 Discussion…………………………………………………………………………9 Acknowledgments………………………………………………………………..10 References………………………………………………………………………..10 Chapter 2: Poor Taxon Sampling, Poor Character Sampling, and Non-Repeatable Analyses of a Contrived Dataset do not Provide a More Credible Estimate of Insect Phylogeny: A Reply to Kjer……………………………………………………..……………………12 Introduction………………………………………………...…………………….13 Empirical Issues……………………………………………………………...…..14 viii Wealth of Data..………………………………………………………………….16 Taxon Sampling………………………………………………………………….17 Basal Pterygotes – Group of Interest……………………………………….…....20 A Specific Example…………………………………………………………..….22 Analytical Issues……………………………………………...………………….23 Conclusions………………………………………...…………………………….30 Acknowledgments………………………………………………………………..31 References………………………………………………………………………..33 Chapter 3: Phylogeny of Ephemeroptera (mayflies) based on molecular evidence……....…………35 Introduction……………………………………………………………..………..37 Material and Methods……………………………………………………..….….42 Results……………………………………………………………………...…….45 Discussion…………………………………………………………………..……47 Conclusion……………………………………………………………………….54 Acknowledgments………………………………………………………………..55 References………………………………………………………………………..56 Figure Legend……………………………………………………………………58 Tables………………………………………………………...…………………..60 Figures………………………………………………………...………………….67 Chapter 4: Combined molecular and morphological Phylogeny of Ephemerellidae (Ephemeroptera) and its position within Pannota………………………………………………………..…73 ix Introduction……………………………………………………………..………..75 Material and Methods……………………………………………………...…….78 Results……………………………………………………………………...…….81 Discussion…………………………………………………………………..……83 Conclusion……………………………………………………………………….85 Acknowledgments………………………………………………………………..86 References………………………………………………………………………..87 Figure Legend……………………………………………………………………90 Tables………………………………………………………...…………………..91 Figures………………………………………………………...………………….93 x Cladistics Cladistics 19 (2003) 432–442 www.elsevier.com/locate/yclad The problem with ‘‘the Paleoptera Problem:’’ sense and sensitivity T. Heath Ogden* and Michael
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