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Phylogenetic Impressions of Reproductive and Genomic

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Phylogenetic Impressions of Reproductive and Genomic THE EVOLUTION OF REPRODUCTIVE AND GENOMIC DIVERSITY IN RAY-FINNED FISHES by JUDITH ELIZABETH MANK (Under the Direction of John C. Avise) ABSTRACT Using comparative phylogenetic methods, I examined several current hypotheses and patterns in the evolution of reproductive and genomic diversity on a supertree for the ray-finned (Actinopterygii) fishes. The topics examined include the evolution of parental care and the implication of viviparity, the evolution of male mating strategies, the evolution of sex determining mechanisms and the relationship between sex chromosomes and male ornaments, evolutionary genomics and the role of genome dynamics in cladogenesis, and the role of sexual selection in increasing taxonomic diversity. Regarding reproductive diversity, the Actinopterygii show remarkable convergence in all traits examined (parental care, internal gestation, male alternative reproductive strategies, and sex determining mechanisms). Similar parental care and male reproductive behaviors in diverse species may be caused by convergent selection on the same suite of gonadotropic hormones. Sexual selection is a major force in the evolution of both parental care and male mating strategies, though sexual selection is not correlated with sex determining mechanisms, it generally acts to increase taxonomic diversity. Internal gestation, though a complex adaptions, has originated multiple independent times throughout the Actinopterygii, and there is no evidence that, once evolved, it has ever been lost from a lineage. This may be because the evolution of viviparity is correlated with cladogenetic expansions. Genomically, actinopterygiian fishes exhibit highly dynamic genomes, possibly due to transposon activity, changes in insertion to deletion ratios, cytogenetic rearrangement, origin and dissolution of sex chromosomes, and gene and genome duplication. This dynamicism may be a factor in the radiation of the teleosts, either by fostering adaptive radiations or via reciprocal silencing. Unexpectedly, the genome dynamics of this clade do not seem to effect higher-level genomic scaffolding, as assessed by somatic chromosome counts. Chromosome complements in the ray-finned fishes are quite stable over vast stretches of evolutionary time. INDEX WORDS: Parental care, Sex determination, Genomics, Mating systems THE EVOLUTION OF REPRODUCTIVE AND GENOMIC DIVERSITY IN RAY-FINNED FISHES By JUDITH ELIZABETH MANK B.A., The University of Florida, 1997 M.S., The Pennsylvania State University, 2001 A Dissertation Submitted to the Graduate School Faculty of the University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY Athens, Georgia 2006 © 2006 Judith Elizabeth Mank All Rights Reserved THE EVOLUTION OF REPRODUCTIVE AND GENOMIC DIVERSITY IN RAY-FINNED FISHES by JUDITH ELIZABETH MANK Major Professor: John Avise Committee: Michael Arnold Daniel Promislow Kenneth Ross John Wares Electronic Version Approved Maureen Grasso Dean of the Graduate School University of Georgia May 2006 ACKNOWLEDGEMENTS No one finishes a Ph.D. without considerable help from others, and I am no exception. Many people have contributed in a variety of ways to this endeavor, and I am grateful to all of them. I thank my advisor, John Avise, for providing a great environment and enormous freedom for me over the last few years. He never dissuaded me from pursuing an idea, generously offered many of his own, and spent countless hours honing the final manuscripts. In many respects, the words in this dissertation are more his than mine, and his help has been invaluable. Daniel Promislow offered assistance, advice, and ideas, going far and beyond the typical role of committee member in order to help me learn the art and science of comparative analysis. His initial suggestion of a study on the evolution of sex determination in fishes set me on the path to this dissertation (it all began as a scribble on my written exams). Daniel has also been a contentious mentor, and helped me in many other professional regards. For this, and everything else, I thank him. My other committee members, Ken Ross, Mike Arnold, and Marjorie Asmussen, kept me on track, kindly grilled me during written and oral exams, and contributed to helpful discussions. Marjorie, I miss you, and I still keep expecting to hear you in the halls. John Wares consented in my fourth year to serve on my committee, and made every effort to understand and contribute to my dissertation research, and for that I am especially grateful. The other past and present members of the Avise lab, namely DeEtte Walker, Beth Dakin, Brady Porter, Andrei Tantarenkov, Mark Mackiewicz, and Felipe Barretto suffered through many tedious editorial lab meetings, listened to repeated student seminars and practice iv talks, and provided moral support, advice, and technical assistance, all of which is much appreciated. Without the efforts of Dave Brown, the computational analyses described here, and my other work at UGA would still likely be cycling. Dave was always willing to help me push the computational envelope, and his efforts to fix software problems, help me find hardware options, and to generally free me from computational limitations made this work possible. My fellow graduate students in the Genetics department offered technical help, the occasional steam valve, and frequent humorous diversions. I wish you all of you the best of luck in everything. My family gave me unwavering love and encouragement, even when they weren’t sure why I was still in school, or when (if ever) I would finally be finished. My mom, as always, was astonishing in her enthusiasm, and I can’t imagine how much harder this would have been without her. She is the most amazing role model and cheerleader. My grandmother kept me on her educational welfare rolls far longer than was seemly, sending me a monthly $10, an encouraging note, and sometimes a hand-drawn piece of art, and I loved it. Boo acted as a paperweight for many of the manuscripts and books that I read, and worked frequently to keep them in line. Her herculean efforts are much appreciated. For the analysis of sex determination, I would like to thank Michael Hardman for assistance regarding catfish phylogeny, Mark Pagel for consultation and advice regarding DISCRETE, and Arne Mooers for helpful suggestions. For the analysis of parental care and sexual selection, I’m grateful to Victor Springer and Jessica Kissinger for advice and suggestions, as well as Donn Eric Rosen and Charles Breder for their wonderful book, Modes of Reproduction in Fishes, which saved me countless hours at the library gathering data points. v Dave Hall, and his work with Mark Kirkpatrick sparked the analysis of sexual selection and sex chromosomes. They both offered searing statistical expertise throughout the analysis and manuscript preparation. Arne Mooers offered very helpful comments on the analysis of cladogenesis and diversification, going so far as to sign his name to his review of the work, and patiently answering all my subsequent questions. Mark Kirkpatrick helped a great deal in a few early discussions about the role of sexual selection and taxonomic diversity. The University of Georgia made my first years at UGA much easier through a Graduate School Fellowship, and the taxpayers of America chipped in later to support my work through an NIH training grant (yes, this does mean that American taxpayers funded research on infidelity, promiscuity, and lewd attire). In my last year, the American Association of University Women Educational Foundation provided a dissertation completion grant, and made possible this compendium, as well as the completion of the related manuscripts. All of these sources of support freed me from the chore of having to work for my money, and they are much appreciated. Thank you, everyone, for all your help and encouragement. vi TABLE OF CONTENTS PAGE ACKNOWLEDGEMENTS ………………………………………………………..iv LIST OF TABLES …………………………………………………………………xii LIST OF FIGURES …………………………………………………………..……xiv CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW: THE EVOLUTION OF DIVERSITY IN RAY-FINNED FISHES…………...…........…1 Introduction……………………………………………………...…2 Goals of This Dissertation……………………………..……...……3 Significance of the Work Presented Here………………………...…4 References Cited…………………………………………….....……6 2 EVOLUTION OF ALTERNATIVE MECHANISMS OF SEX DETERMINATION IN ACTINOPTETRYGIIAN FISHES…...…. 8 Abstract………………………………………………………...…...9 Introduction……………………………………………………....…10 Material and Methods…………………………………………….…11 Results…………………………………………………………....…12 Discussion…………………………………………………………...18 References Cited…………………………………………..……...…30 3 SEX CHROMOSOMES AND MALE ORNAMENTS: A COMPARATIVE EVALUATION IN RAY-FINNED FISHES .….40 vii Abstract……………………………………………………...…..….41 Introduction…………………………………………………………42 Materials and Methods………………………………………...……44 Results and Discussion…………………………………………...…46 References Cited………………………………………………….…52 4 PHYLOGENETIC PERSPECTIVES ON THE EVOLUTION OF PARENTAL CARE IN RAY-FINNED FISHES………………...…57 Abstract……………………………………………………………..58 Introduction……………………………………………...….………60 Material and Methods……………………………………...….……62 Results……………………………………………………...…….…66 Discussion…………………………………………………….…….72 References Cited…………………………………………….………81 5 COMPARATIVE PHYLOGENETIC ANALYSIS OF MALE ALTERNATIVE REPRODUCTIVE TACTICS IN RAY-FINNED FISHES………………………………………………...……………89 Abstract…………………………………………...……………...…90 Introduction…………………………………….………………...…91 Material and Methods…………………………….……………...…93 Results………………………………………………….………...…94
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