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Genetic Variation in Fast-Evolving East African Cichlid Fishes: an Evolutionary Perspective

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Genetic Variation in Fast-Evolving East African Cichlid Fishes: an Evolutionary Perspective GENETIC VARIATION IN FAST-EVOLVING EAST AFRICAN CICHLID FISHES: AN EVOLUTIONARY PERSPECTIVE A Dissertation Presented to The Academic Faculty By Yong-Hwee Eddie Loh In Partial Fulfillment Of the Requirements for the Degree Doctor of Philosophy in Biology Georgia Institute of Technology August 2011 GENETIC VARIATION IN FAST-EVOLVING EAST AFRICAN CICHLID FISHES: AN EVOLUTIONARY PERSPECTIVE Approved by: Dr. Todd Streelman, Advisor Dr. King Jordan School of Biology School of Biology Georgia Institute of Technology Georgia Institute of Technology Dr. Soojin Yi, Co-Advisor Dr. James Thomas School of Biology Department of Human Genetics Georgia Institute of Technology Emory University Dr. John McDonald School of Biology Georgia Institute of Technology Date Approved: June 14, 2011 To my dear parents Eric and Florence... ACKNOWLEDGEMENTS I would like to express my sincere appreciation to my academic advisor Dr Todd Streelman for his guidance over these years. His infectious motivation and enthusiam spurred me to continually push beyond established boundaries, allowing me to grow both professionally and personally. I would like to thank my co-advisor Dr Soojin Yi for her unwavering support, advice and encouragement, which started from the very first days of my arrival at Georgia Tech. I would also like to thank my committee members Dr King Jordan, Dr John McDonald and Dr James Thomas for their valuable advice and constructive feedback on my research. Also to Dr Byrappa Venkatesh and Dr Sydney Brenner, I am grateful for the early opportunites to work with them, which inspired me onto this great career. I am grateful to my friends spread all around the world, and especially those here from the Streelman and Yi Labs, for all the fun, laughter, and of course science, without which this journey wouldn’t have been as eventful and fulfilling. Most of all, I am thankful to my family, from both back in Singapore and here with me in Atlanta. Their love, understanding, support and encouragement made all these work possible. iv TABLE OF CONTENTS ACKNOWLEDGEMENTS..................................................................................................v LIST OF TABLES..............................................................................................................ix LIST OF FIGURES............................................................................................................x LIST OF ABBREVIATIONS..............................................................................................xi SUMMARY......................................................................................................................xii CHAPTER 1: INTRODUCTION.........................................................................................1 CHAPTER 2: COMPARATIVE ANALYSIS REVEALS SIGNAURES OF DIFFERENTIATION AMID GENOMIC POLYMORPHISM IN LAKE MALAWI CICHLIDS.....................................................................................4 2.1 Abstract..................................................................................................................4 2.2 Background............................................................................................................5 2.3 Results...................................................................................................................7 2.3.1 Sequence assembly......................................................................................7 2.3.2 Gene content and coverage..........................................................................8 2.3.3 Clustering and alignment..............................................................................9 2.3.4 Segregating site..........................................................................................11 2.3.5 Validation and generality of SNPs..............................................................13 2.3.6 Genetic polymorphism and divergence at multiple scales..........................15 2.3.7 Genetic clustering and ancestry..................................................................17 2.4 Discussion............................................................................................................19 2.4.1 Cichlid species exhibit genomic polymorphism...........................................19 2.4.2 Genomic polymorphism and the divergence of Malawi cichlids..................21 2.4.3 Discovery for evolutionary biology..............................................................22 2.5 Materials and methods........................................................................................24 2.5.1 Samples......................................................................................................24 v 2.5.2 Trace sequences........................................................................................24 2.5.3 Sequence pre-processing and assembly....................................................25 2.5.4 Similarity search and alignment..................................................................26 2.5.5 Protein-coding sequence identification.......................................................27 2.5.6 Evolutionary sequence divergence among JGI species.............................27 2.5.7 Genotyping and validation of SNPs............................................................28 2.5.8 Genetic differentiation within and among lineages.....................................29 2.5.9 Genomic assignment..................................................................................29 2.6 Acknowledgements..............................................................................................29 2.7 References...........................................................................................................30 CHAPTER 3: EARLY ORIGINS OF GENETIC VARIATION IN LAKE MALAWI CICHLIDS..................................................................................................37 3.1 Abstract................................................................................................................37 3.2 Introduction..........................................................................................................38 3.3 Materials and methods........................................................................................41 3.3.1 Fish samples and genotyping.....................................................................41 3.3.2 Coincident polymorphism...........................................................................43 3.3.3 Genetic clustering.......................................................................................43 3.3.4 Genetic differentiation.................................................................................44 3.4 Results and discussion........................................................................................44 3.4.1 Genotype data............................................................................................44 3.4.2 Origins of Lake Malawi polymorphism........................................................46 3.4.3 Genetic clustering of East African cichlids..................................................52 3.4.4 Genetic admixture in cichlid species...........................................................55 3.4.5 Genetic divergence in Lake Malawi cichlids...............................................57 3.5 Conclusion...........................................................................................................61 vi 3.6 Acknowledgements..............................................................................................63 3.7 References...........................................................................................................63 CHAPTER 4: EVOLUTION OF MICRORNAS AND THE DIVERSIFICATION OF SPECIES...................................................................................................69 4.1 Abstract................................................................................................................69 4.2 Introduction..........................................................................................................70 4.3 Materials and methods........................................................................................72 4.3.1 Lake Malawi Genomes...............................................................................73 4.3.2 miRNA Gene Detection..............................................................................73 4.3.3 3’-UTR Annotation......................................................................................74 4.3.4 miRNA Target Prediction............................................................................75 4.3.5 Target SNP Density Calculations...............................................................76 4.3.6 3’-UTR Re-sequencing, Alignment and Target Prediction.........................76 4.3.7 Minor Allele Frequencies of SNPs in Re-sequenced 3’-UTRs...................77 4.3.8 Genetic Differentiation of High-MAF Target SNPs in Re-Sequenced 3’- UTRs..........................................................................................................78 4.4 Results................................................................................................................78 4.4.1 miRNA Prediction.......................................................................................78 4.4.2 Polymorphism in Cichlid miRNA Targets...................................................79 4.4.3 MAFs and Genetic Differentiation
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