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Cichlids As a Model for the Evolution of Visual Sensitivity Tyrone Clifford Spady University of New Hampshire, Durham

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Cichlids As a Model for the Evolution of Visual Sensitivity Tyrone Clifford Spady University of New Hampshire, Durham University of New Hampshire University of New Hampshire Scholars' Repository Doctoral Dissertations Student Scholarship Spring 2006 Cichlids as a model for the evolution of visual sensitivity Tyrone Clifford Spady University of New Hampshire, Durham Follow this and additional works at: https://scholars.unh.edu/dissertation Recommended Citation Spady, Tyrone Clifford, "Cichlids as a model for the evolution of visual sensitivity" (2006). Doctoral Dissertations. 331. https://scholars.unh.edu/dissertation/331 This Dissertation is brought to you for free and open access by the Student Scholarship at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. CICHLIDS AS A MODEL FOR THE EVOLUTION OF VISUAL SENSITIVITY BY TYRONE CLIFFORD SPADY B.S., University of Maryland Baltimore County, 2000 DISSERTATION Submitted to the University of New Hampshire In Partial Fulfillment of the Requirements for the Defense of Doctor of Philosophy in Zoology May, 2006 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. UMI Number: 3217442 INFORMATION TO USERS The quality of this reproduction is dependent upon the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleed-through, substandard margins, and improper alignment can adversely affect reproduction. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note will indicate the deletion. ® UMI UMI Microform 3217442 Copyright 2006 by ProQuest Information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. ProQuest Information and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This dissertation has been examined and approved. Dissertation Director, Dr. Karen L. Carleton, Research Associate Professor of Zoology Dr. Rick H. Cote, Professor of Biochemistry and Molecular Biology Dr. Thomas D. Kocher, Professor of Zoology and Genetics Dr. Michelle P. Scott, Professor of Zoology Dr. Gil Rosenthal, Assistant Professor of Biology, Texas A&M University / ? - - ij - Q _ c , Date ii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOWLEDGEMENTS I first thank, my mentor and advisor, Karen Carleton, for helping me to find my voice as a scientist and for being “unwaveringly supportive, inexhaustibly available, and disarmingly open.” I am also grateful to my coadvisor, Tom Kocher, for being the perfect complement to Karen Carleton. Together they created a stimulating and challenging intellectual environment. I am particularly thankful to current and former labmates and other UNH graduate students for helping to make New Hampshire my home. I thank Rick Cote and particularly Michelle Scott for their advice and encouragement, both professionally and personally during the course of my graduate studies. I also thank Gil Rosenthal for his time and willingness to serve on my dissertation committee. I thank my collaborators. Thank you to family, friends, and previous teachers and mentors for providing me with a life full of opportunities. This work has been supported by the UNH Graduate School, UNH Zoology Department, and NSF. iii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS A CKNOWLEDGEMENTS............................................................................................iii LIST OF TABLES..........................................................................................................vi LIST OF FIGURES.........................................................................................................vii ABSTRACT....................................................................................................................viii CHAPTER PAGE INTRODUCTION............................................................................................................1 I. ADAPTIVE MOLECULAR EVOLUTION IN THE OPSIN GENES OF RAPIDLY SPECIATING CICHLID SPECIES..................................................................................5 A. Abstract............................................................................................................5 B. Introduction......................................................................................................7 C. Methods ............................................. 11 D. Results............................................................................................................. 15 E. Discussion ........................................................................................................20 F. Conclusions ......................................................................................................25 II. EVOLUTION OF THE CICHLID VISUAL PALETTE THROUGH ONTOGENETIC SUBFUNCTIONALIZATION OF THE OPSIN GENE ARRAYS...36 A. Abstract...........................................................................................................36 B. Introduction .....................................................................................................38 C. Methods ...........................................................................................................41 iv Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. D. Results 46 E. Discussion ........................................................................................................51 III. DIFFERENCES IN VISUAL SENSITIVITY AMONG THE LAB1DOCHROM1S GENUS OF RAPIDLY SPECIATING LAKE MALAWI CICHLIDS........................... 64 A. Abstract............................................................................................................64 B. Introduction ......................................................................................................66 C. Methods ............................................................................................................69 D. Results..............................................................................................................72 E. Discussion .........................................................................................................74 IV. EXTENSIVE GENE DUPLICATION OF FISH CONE OPSIN GENES............... 85 A. Abstract............................................................................................................85 B. Introduction ......................................................................................................87 C. Methods ............................................................................................................89 D. Results..............................................................................................................91 E. Discussion .........................................................................................................95 V. WHAT CAN CICHLIDS REVEAL ABOUT THE RELATIONSHIP OF COLOR VISION AND ECOLOGY?............................................................................................105 LIST OF REFERENCES................................................................................................. 110 APPENDIX..................................................................................................................... 122 v Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES 1.1 Study Species .............................................................................................................27 1.2 Site variable LRT results ............................................................................................28 1.3 Nonsynonymous/synonymous rate ratio ....................................................................29 1.4 Branch-site variable LRT results ...............................................................................30 1.5 Comparison of PAML predictions and possible tuning sites .....................................31 1.6 Possible opsin tuning sites based on previous functional and structural studies 33 2.1 Percentage of total opsin expression ..........................................................................56 2.2 Comparison of tilapia and Lake Malawi cichlid visual pigments..............................57 3.1 STUDY SPECIES................................. 79 3.2 Labidochromis relative cone opsin gene expression as determined by real-time RT- PCR..................................................................................................................................80 3.3 Labidochromis cone visual pigment sensitivities determined by MSP, ± 1 SD 81 3.4 Comparison of the visual pigment classes found among cichlids..............................82 4.1 Divergence estimates for each opsin duplication ......................................................99 vi Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES 1.1 Cichlid opsin unrooted neighbor
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