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©Copyright 2008 Joseph A. Ross the Evolution of Sex-Chromosome Systems in Stickleback Fishes

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©Copyright 2008 Joseph A. Ross the Evolution of Sex-Chromosome Systems in Stickleback Fishes ©Copyright 2008 Joseph A. Ross The Evolution of Sex-Chromosome Systems in Stickleback Fishes Joseph A. Ross A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2008 Program Authorized to Offer Degree: Molecular and Cellular Biology University of Washington Graduate School This is to certify that I have examined this copy of a doctoral dissertation by Joseph A. Ross and have found that it is complete and satisfactory in all respects, and that any and all revisions required by the final examining committee have been made. Chair of the Supervisory Committee: Catherine L. Peichel Reading Committee: Catherine L. Peichel Steven Henikoff Barbara J. Trask Date: In presenting this dissertation in partial fulfillment of the requirements for the doctoral degree at the University of Washington, I agree that the Library shall make its copies freely available for inspection. I further agree that extensive copying of the dissertation is allowable only for scholarly purposes, consistent with “fair use” as prescribed in the U.S. Copyright Law. Requests for copying or reproduction of this dissertation may be referred to ProQuest Information and Learning, 300 North Zeeb Road, Ann Arbor, MI 48106-1346, 1-800-521-0600, to whom the author has granted “the right to reproduce and sell (a) copies of the manuscript in microform and/or (b) printed copies of the manuscript made from microform.” Signature Date University of Washington Abstract The Evolution of Sex-Chromosome Systems in Stickleback Fishes Joseph A. Ross Chair of the Supervisory Committee: Affiliate Assistant Professor Catherine L. Peichel Department of Biology The genetical and physical degeneration of sex chromosomes in many diverse taxa has been described, yet the mechanisms initiating the degenerative process have not been characterized extensively by studying young sex-chromosome systems. Following the genetic identification of an XY pair in threespine sticklebacks,Gasterosteus aculea- tus, I conducted sequence analyses and a cytogenetic characterization of the Y chromo- some. I found that the chronologically young threespine Y has a nonrecombining region that exhibits sequence characteristics expected of evolved sex chromosomes, including an accumulation of repetitive sequence elements, reduced homology with the X, and the presence of inversions and deletions. These findings fulfill predictions that repetitive DNA and inversions might initiate loss of recombination on a sex chromosome. Efforts to clone and sequence the threespine Y for further analysis have thus far yielded 1.9 Mbp of sequence. My comparative cytogenetic studies have identified the presence of three previously unknown heteromorphic sex-chromosome systems in stickleback species. The identification of two independent 1X X2Y/XX systems having relationships to XY sex-chromosome systems in sister taxa along with the presence of a ZW pair in stickle- back species diverged less than twenty million years have stimulated research addressing existing theories of sex chromosome-autosome fusions and will permit the characteriza- tion of the transition between sex-chromosome systems and the genetic evaluation of the role of chromosomal rearrangements in speciation. These findings reflect the lability of sex-determination mechanisms and sex-chromosome systems in fish and strengthen the stickleback family of fish as a model system in which to study the evolution of sex deter- mination and sex chromosomes. TABLE OF CONTENTS List of Figures…………………………………………………………………………….. i i List of Tables…………………………………………………………………………….. iii Preface…………………………………………………………………………………… iv Chapter 1. Background…………………………………………………………………… 1 Mechanisms of Sex Determination……………………………………………….. 2 Identifying the Presence of GSD…………………………………………………. 3 Vertebrate Sex-chromosome Systems…………………………………………….. 4 Evolution of Sex-determining Factors……………………………………………. 8 Sex-chromosome Evolution……………………………………………………... 10 Mechanisms of Reduced Recombination………………………………………... 15 Sex Determination and Sex Chromosomes in Stickleback Fishes………………. 17 Chapter 2. Characteristics of an XY Pair in Threespine Sticklebacks…………………... 2 0 Introduction……………………………………………………………………… 20 Materials and Methods…………………………………………………………... 20 Results…………………………………………………………………………… 22 Discussion……………………………………………………………………….. 31 Chapter 3. Cloning the Threespine Stickleback X and Y Chromosomes……………….. 33 Introduction……………………………………………………………………… 33 Materials and Methods…………………………………………………………... 35 Results and Discussion………………………………………………………….. 39 Chapter 4. Cytogenetic Characterization of the Threespine Y Chromosome…………… 52 Introduction……………………………………………………………………… 52 Materials and Methods…………………………………………………………... 55 Results…………………………………………………………………………… 60 Discussion……………………………………………………………………….. 68 Chapter 5. Evolution of Sex Determination and Sex Chromosomes in Sticklebacks…... 74 Introduction……………………………………………………………………… 74 Materials and Methods…………………………………………………………... 78 Results…………………………………………………………………………… 80 Discussion……………………………………………………………………….. 96 Chapter 6. Summary and Future Directions……………………………………………. 1 1 5 Materials and Methods…………………………………………………………. 117 Identification ofSEX in Sticklebacks…………………………………………... 117 Comparative Studies…………………………………………………………… 126 The Future of Sex Chromosomes…………………………………………….... 129 Bibliography…………………………………………………………………………… 130 i LIST OF FIGURES Figure Number Page 1. Conservation of genetic sex determination across taxa.……………………………….. 9 2. The evolution of degenerate sex chromosomes.……………………………………… 12 3. Phylogeny of North American stickleback fishes.……………………………………. 18 4. Linkage maps of the threespine stickleback X and Y chromosomes.………………… 2 3 5. Assemblies of the X and Y chromosome Idh BAC sequences.………………………. 25 6. Vista plot of the X and Y Idh BAC sequence assemblies.……………………………. 27 7. Dot plots of Idh sequence assemblies from the X and Y.……………………………... 2 9 8. STS content map of the Idh contig of CH213 BAC clones.………………………….. 34 9. BAC minimum tiling path (MTP) from Idh X chromosome walk in CH213………... 42 10. BAC MTP from Idh Y chromosome walk in CH213.………………………………. 44 11. BAC MTP at Stn191 in CH213.……………………………………………………... 4 4 12. BAC MTP at Stn192 in CH213.……………………………………………………... 4 4 13. BAC MTPs from chromosome walks in CH215.…………………………………… 50 14. Genetic and sequence maps of the threespine X.……………………………………. 5 6 15. The threespine Y is heteromorphic.…………………………………………………. 62 16. Threespine stickleback male karyogram.……………………………………………. 6 3 17. Deletion on the threespine Y.………………………………………………………... 64 18. FISH-based cytogenetic maps of the threespine X and Y.…………………………... 6 5 19. Pericentric inversion on the threespine Y.…………………………………………… 6 6 20. Refining probe orders on the threespine X and Y.…………………………………... 67 21. Parsimony model for the evolution of the threespine Y.…………………………….. 6 8 22. Linkage maps of the black-spotted sex chromosome.………………………………. 83 23. Karyograms of black-spotted sticklebacks.…………………………………………. 84 24. FISH analyses of LG12 and LG19.………………………………………………….. 8 6 25. Ninespine stickleback karyograms.…………………………………………………. 87 26. Certain LG19 FISH probes do not hybridize to the black-spotted Y.……………….. 89 27. Genetic maps of Japan Sea LG9 and LG19.………………………………………… 9 0 28. FISH demonstration of LG9-19 fusion in Japan Sea males.………………………… 9 1 29. Relationship between LG9 and LG19 in Japan Pacific Ocean males.………………. 9 3 30. FISH analyses of LG12 and LG19 in brook and fourspine sticklebacks.…………… 9 6 31. Brook stickleback karyograms.……………………………………………………… 9 7 32. Fourspine stickleback karyograms.………………………………………………….. 9 8 33. BAC fingerprint mapping of CH215 contigs.……………………………………… 121 34. Use of FISH to assign chromosomal origin of probes.…………………………….. 123 ii LIST OF TABLES Table Number Page 1. Repeat content on the threespine X and Y at Idh.…………………………………….. 2 8 2. Stn194 alleles in threespine sticklebacks.…………………………………………….. 41 3. Initial CH215 BAC library screen clones.……………………………………………. 48 4. Sources of FISH probes.……………………………………………………………… 58 5. SEX-linked threespine and ninespine markers used for genotyping………………….. 8 1 6. Marker genotype-sex phenotype associations in black-spotted sticklebacks.….…….. 82 7. Karyotype data for stickleback fishes.………………………………………………... 85 8. Markers used for genotyping brook and fourspine stickleback crosses.……………... 95 iii PREFACE It has been exciting and a pleasure to have helped develop stickleback fish as model systems for studying the dynamic and unpredictable path that sex chromosomes tread and to have been a part of the development of sticklebacks as model genetic and genomic organisms. The process of refining and improving the techniques for cloning a sex chromosome, creating custom computational tools for analyzing sequence data, and developing FISH techniques for sticklebacks were particularly rewarding by allowing me to explore diverse disciplines. I feel particularly blessed to have developed a project that I was excited daily to engage because I knew I could discover something exciting and novel at any point. While I hate to leave behind so many questions, the answers to which seem to be just around the corner, it is with great pride and satisfaction that I do so because it is as a result of my research that these questions are possible for another generation in the Peichel lab to ask. Joseph A. Ross 1 August 2008 Seattle, Washington iv ACKNOWLEDGEMENTS Data in Chapter Two were published previously as Peichel et al. (2004)
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