W&M ScholarWorks Dissertations, Theses, and Masters Projects Theses, Dissertations, & Master Projects 1998 The phylogeny of coleoid cephalopods inferred from molecular evolutionary analyses of the cytochrome c oxidase I, muscle actin, and cytoplasmic actin genes David Bruno Carlini College of William and Mary - Virginia Institute of Marine Science Follow this and additional works at: https://scholarworks.wm.edu/etd Part of the Genetics Commons, Molecular Biology Commons, and the Zoology Commons Recommended Citation Carlini, David Bruno, "The phylogeny of coleoid cephalopods inferred from molecular evolutionary analyses of the cytochrome c oxidase I, muscle actin, and cytoplasmic actin genes" (1998). Dissertations, Theses, and Masters Projects. Paper 1539616597. https://dx.doi.org/doi:10.25773/v5-3pyk-f023 This Dissertation is brought to you for free and open access by the Theses, Dissertations, & Master Projects at W&M ScholarWorks. 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Reproduced with with permission permission of the of copyright the copyright owner. owner.Further reproductionFurther reproduction prohibited without prohibited permission. without permission. THE PHYLOGENY OF COLEODD CEPHALOPODS INFERRED FROM MOLECULAR EVOLUTIONARY ANALYSES OF THE CYTOCHROME C OXIDASE I, MUSCLE ACTIN, AND CYTOPLASMIC ACTIN GENES A Dissertation Presented to The Faculty of the School of Marine Science The College of William and Mary in Virginia In Partial Fulfillment Of the Requirements for the Degree of Doctor of Philosophy by David Bruno Carlini 1998 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. UMI Number: 9903260 UMI Microform 9903260 Copyright 1998, by UMI Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. UMI 300 North Zeeb Road Ann Arbor, MI 48103 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. APPROVAL SHEET This dissertation is submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy David B. Carlini Approved, August 1998 ' A ~ £ - C\,M> John E. Graves, Ph.D. Committee Chairman/Advisor /Elizabeth A. Canuel, Ph.D. l£o U s . Roger L. Mann, Ph.D. Kimberly S. Reece, Ph.D. — -------- Michael Vecchione, Ph.D. National Museum of Natural History Smithsonian Institution, Washington, D.C. ' J£_ Richard E. Yoyng, Ph.! Department of Oceanography University of Hawaii, Honolulu ii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS Page ACKNOWLEDGMENTS vi LIST OF TABLES viii LIST OF FIGURES ix ABSTRACT xiii GENERAL INTRODUCTION 2 Morphological Systematics of the Coleoidea 2 Molecular Systematics of the Coleoidea 7 Phylogenetic Analysis 11 Phylogenetic Hypotheses Tested 13 CHAPTER 1. PHYLOGENETIC RELATIONSHIPS OF COLEOID CEPHALOPODS INFERRED FROM THE MOLECULAR EVOLUTION OF THE MITOCHONDRIAL CYTOCHROME C OXIDASE I GENE 19 INTRODUCTION 20 MATERIALS AND METHODS 25 Taxonomic Sampling 25 DNA Extraction, PCR Amplification, and Cloning 25 Manual Sequencing 27 Automated Sequencing 27 Data Analysis 28 RESULTS 33 Sequence Variation and Divergence 33 iii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Phylogenetic Relationships 35 DISCUSSION 40 Sequence Variation and Divergence 40 Phylogenetic Relationships 41 CHAPTER 2. PHYLOGENETIC RELATIONSHIPS OF COLEOID CEPHALOPODS INFERRED FROM THE MOLECULAR EVOLUTION OF TWO PARALOGOUS GENES FROM THE ACTIN GENE FAMILY 82 INTRODUCTION 83 MATERIALS AND METHODS 88 Taxonomic Sampling 88 PCR Amplification, Cloning, and Sequencing 88 Data Analysis 89 RESULTS 93 Actin Isoforms 93 Actin I Sequence Variation and Divergence 94 Actin IT Sequence Variation and Divergence 95 Phylogenetic Relationships - Actin I 97 Phylogenetic Relationships - Actin II 100 DISCUSSION 103 The Actin Gene Family of Coleoid Cephalopods 103 Sequence Variation and Divergence 107 Phylogenetic Relationships 109 CHAPTER 3. PHYLOGENETIC RELATIONSHIPS OF COLEOID CEPHALOPODS INFERRED FROM THE ANALYSIS OF COMBINED ACTIN I, ACTIN E, AND CYTOCHROME C OXIDASE I DATA SETS AND A COMPARISON OF THEIR PATTERNS OF MOLECULAR EVOLUTION 180 INTRODUCTION 181 iv Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. MATERIALS AND METHODS . .. 186 Taxonomic Sampling 186 Data Analysis 186 RESULTS 191 Sequence Variation and Divergence 191 Codon Usage 192 Phylogenetic Analyses 193 DISCUSSION 199 Sequence Variation and Divergence 199 Codon Usage 200 Phylogenetic Relationships 201 CONCLUSIONS 245 Octopodiformes and Decapodiformes 245 Octopoda 245 Sepioidea and Myopsida 248 Oegopsida LITERATURE CITED 257 VITA 273 v Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGMENTS This study could not have been accomplished without the help of many people, most of whom I attempt to list below-I apologize in advance for any omissions. I extend my sincere thanks to my dissertation committee. I am indebted Dr. John Graves, my major advisor, for his encouragement, support, and advice through the duration of this project. Dr. Kimberly Reece deserves special thanks for generously sharing her molecular expertise and for her consistent willingness to help in all aspects of this research project. I am grateful to Drs. Michael Vecchione and Richard Young for inspiring a fervent interest in cephalopod biology and for answering all my questions promptly and patiently. I also thank them for their immense help in collecting specimens and for introducing me to cephalopod researchers throughout the world. Thanks to Drs. Roger Mann and Elizabeth Canuel for critically reviewing this dissertation and for their helpful suggestions. I thank the following people for their help in the molecular aspects of this project: Dr. Kimberely Reece, Jan McDowell, Nancy Stokes, Dr. Peter Cooper, and all past and present members of the Fisheries Genetics lab. Dr. Mark Siddall, Dr. Andy Anderson, and Dr. Emmett Duffy provided invaluable assistance with phylogenetic methods. The cephalopod specimens included in this study could not have been obtained without the generous aid of Dr. Richard Young, Dr. Michael Vecchione, Dr. Yasunori Sakurai, Dr. Brad Seibel, Tim Stranks, Amanda Reid, David Woodbury, Dr. Jayson Semmens, Matt Parry, Scott Herke, Dr. John Bower, Ian Bartol, Liz Shea, Dr. Laure Bonnaud, Dr. Renata Boucher-Rodoni, Dr. Steven O'Shea, and Dr. Louise Allcock. I also thank the officers and crews of FTS HOKUSEIMARU and R/V DAVID STARR JORDAN. vi Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This dissertation was financially supported by a National Science Foundation Doctoral Dissertation Improvement Grant (DEB-9623353) awarded to D.B. Carlini and J.E. Graves. The research was also supported by a Lemer Gray Fund for Marine Research Grant, a Western Society of Malacologists Student Research Grant in Malacology, and a VIMS Minor Research Grant awarded to D.B. Carlini. I thank my parents, brothers, and sisters for their support and encouragement. I cannot express enough thanks to my wife Amy for her love, commitment, and sacrifice over the past several years. I am also grateful for her long-standing interest in and reverence for the natural world. With her, I have enjoyed many enlightening discussions about biology and evolution. Finally, I must acknowledge our daughter Zoe for serving as a strong, although unwitting, source of inspiration. vii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES Table Page 1. List of specimens used in this study 51