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Molecular and Cellular Bases of Color Pattern Evolution in Cichlid Fishes

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Molecular and Cellular Bases of Color Pattern Evolution in Cichlid Fishes Molecular and cellular bases of color pattern evolution in cichlid fishes Doctoral dissertation for obtaining the academic degree Doctor of Natural Sciences submitted by Liang, Yipeng at the Faculty of Sciences Department of Biology Konstanz, 2020 Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-rkd9iiw5z5k24 Date of the oral examination: 14th July 2020 1. Reviewer: Prof. Dr. Axel Meyer 2. Reviewer: Prof. Dr. Mark van Kleunen ⁕ Table of contents ⁕ Table of contents Table of contents .......................................................................................... i List of Figures ............................................................................................. iv List of Tables ............................................................................................. vii Summary ..................................................................................................... ix Zusammenfassung .................................................................................... xii General Introduction .................................................................................. 1 Cellular and molecular basis of vertebrate color patterns ................................ 1 Cichlid fishes as a model system for studying color pattern formation ........... 4 Objectives of the Thesis ................................................................................. 11 Chapter I Agouti-related Peptide 2 Facilitates Convergent Evolution of Stripe Patterns across Cichlid Fish Radiations ................................. 12 Abstract .......................................................................................................... 12 Main text ........................................................................................................ 13 Materials and Methods ................................................................................... 20 Supplementary Text ....................................................................................... 30 Chapter II Evolutionary Dynamics of Structural Variation at a Key Locus for Color Pattern Diversification in Cichlid Fishes .................... 36 Abstract .......................................................................................................... 36 Introduction .................................................................................................... 37 Materials and Methods ................................................................................... 37 Results ............................................................................................................ 45 Discussion ...................................................................................................... 55 Chapter III The Teleost-Specific Genome Duplication and Color Pattern Evolution in Modern Fishes: Retention of Functional Conservation, Neo-functional Divergence and Sub-functionalization of Agouti Genes .............................................................................................. 58 Abstract .......................................................................................................... 58 Main text ........................................................................................................ 59 Materials and Methods ................................................................................... 66 – i – ⁕ Table of contents ⁕ Chapter IV Neural Innervation as a Potential Trigger of Morphological Color Change and Sexual Dimorphism in Cichlid Fish ..................................................................................................................... 67 Abstract .......................................................................................................... 67 Introduction .................................................................................................... 68 Results ............................................................................................................ 70 Discussion ...................................................................................................... 82 Methods .......................................................................................................... 86 Chapter V Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus . 91 Abstract .......................................................................................................... 91 Introduction .................................................................................................... 92 Results ............................................................................................................ 93 Discussion .................................................................................................... 104 Conclusion ................................................................................................... 109 Materials and Methods ................................................................................. 110 General Discussion .................................................................................. 115 Main contribution ......................................................................................... 115 Future and Outlook ...................................................................................... 121 References ................................................................................................ 123 Acknowledgments ................................................................................... 149 General acknowledgments ............................................................................ 149 Chapter specific acknowledgments .............................................................. 150 Chapter I ....................................................................................................... 150 Chapter II ..................................................................................................... 150 Chapter III .................................................................................................... 150 Chapter IV .................................................................................................... 151 Chapter V ..................................................................................................... 151 Author Contributions ............................................................................. 152 Chapter I ....................................................................................................... 152 Chapter II ..................................................................................................... 152 Chapter III .................................................................................................... 152 – ii – ⁕ Table of contents ⁕ Chapter IV .................................................................................................... 153 Chapter V ..................................................................................................... 153 Supplementary Material ........................................................................ 154 Chapter I ....................................................................................................... 154 Chapter II ..................................................................................................... 172 Chapter III .................................................................................................... 186 Chapter IV .................................................................................................... 190 Chapter V ..................................................................................................... 201 – iii – ⁕ List of Figures ⁕ List of Figures Fig. I.1 Convergent evolution of horizontal stripes across African cichlid radiations. 14 Fig. I.2 Agrp2 controls stripe loss in Lake Victoria cichlids. ........................................ 16 Fig. I.3 Regulatory changes of agrp2 are predictive of convergent stripe evolution..... 17 Fig. I.4 A shared genomic basis of stripes across cichlid radiations.............................. 19 Fig. II.1 Sequence conservation at the agrp2 locus. ...................................................... 45 Fig. II.2 Isoforms of agrp2. ............................................................................................ 46 Fig. II.3 The third exon of agrp2 was tandemly duplicated. ......................................... 50 Fig. II.4 Expression bias towards exon 3a and resurrection of exon 3b ........................ 52 Fig. II.5 Phylogeny of the agrp2 gene across cichlids. .................................................. 53 Fig. II.6 Protein sequence evolution of agrp2 across cichlid fishes. ............................. 54 Fig. II.7 Summary of the evolutionary history of the agrp2 gene. ................................ 55 Fig. III.1 Expression differences of asip1 and agrp2 associate with stripe pattern formation and evolutionary loss across teleost fishes. ................................................... 61 Fig. III.2 Evolution of agouti gene function across teleosts and tetrapods. ................... 64 Fig. IV. 1 Yellow and black morph of Melanochromis auratus. ................................... 68 Fig. IV.2 Chromatophore measurements in scales of yellow and dark morph of M. auratus scales. ...............................................................................................................
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