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Evolution of Oxidative Metabolism in Fishes

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Evolution of Oxidative Metabolism in Fishes EVOLUTION OF OXIDATIVE METABOLISM IN FISHES by Alexander George Little A thesis submitted to the Department of Biology In conformity with the requirements for the degree of Master of Science Queenʼs University Kingston, Ontario, Canada September, 2009 ©Alexander George Little, 2009 Library and Archives Bibliothèque et Canada Archives Canada Published Heritage Direction du Branch Patrimoine de l’édition 395 Wellington Street 395, rue Wellington Ottawa ON K1A 0N4 Ottawa ON K1A 0N4 Canada Canada Your file Votre référence ISBN: 978-0-494-70040-2 Our file Notre référence ISBN: 978-0-494-70040-2 NOTICE: AVIS: The author has granted a non- L’auteur a accordé une licence non exclusive exclusive license allowing Library and permettant à la Bibliothèque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par télécommunication ou par l’Internet, prêter, telecommunication or on the Internet, distribuer et vendre des thèses partout dans le loan, distribute and sell theses monde, à des fins commerciales ou autres, sur worldwide, for commercial or non- support microforme, papier, électronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L’auteur conserve la propriété du droit d’auteur ownership and moral rights in this et des droits moraux qui protège cette thèse. Ni thesis. Neither the thesis nor la thèse ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent être imprimés ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author’s permission. In compliance with the Canadian Conformément à la loi canadienne sur la Privacy Act some supporting forms protection de la vie privée, quelques may have been removed from this formulaires secondaires ont été enlevés de thesis. cette thèse. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n’y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. Abstract " My study investigated the evolution of oxidative metabolism in fishes. While intense selection for, or against, non-synonymous point mutations in coding sequence drives the evolution of mitochondrial OXPHOS genes, genome-specific mechanisms such as gene duplication events can play major roles in the evolution of nuclear OXPHOS genes. My thesis focused on the mitochondrial enzyme cytochrome c oxidase (COX), principally in fish because of their evolutionary origins and functional diversity in terms of energy metabolism. In the first part of my thesis, I examined a highly aerobic group of fishes (billfishes and tunas) to study the evolution of mitochondrial COX genes. Though the study began as a structure-function analysis of COX, my approach changed when my preliminary results called into question the accepted phylogenetic relationships of my species of interest. We generated a robust multigene phylogeny of this group to interpret data in a phylogenetically informative context. Phylogenetic analyses in this group provided us with a framework to study the evolution of mitochondrial OXPHOS genes, but unexpectedly revealed that: 1) billfishes are only distantly related to tunas, and share greater evolutionary affinities with flatfishes (Pleuronectiformes) and jacks (Carangidae), and 2) regional endothermy has evolved in a non-scombroid suborder in teleosts. These results collectively imply that regional endothermy has evolved independently at least twice within teleost fish. The second part of my thesis explored the evolution of the nuclear COX subunits, focusing on their origins in fish. Isoform transcription profiles coupled with phylogenetic analyses for each subunit show that vertebrate isoforms arose from a combination of early whole-genome duplications in basal vertebrates or specific lineages (e.g. teleosts), and more recent ii single gene duplication events. While there is evidence for retained function of some COX orthologues across fishes and mammals, others appear to have diverged in function since their earlier radiation, possibly contributing novel evolutionary functions. Together these two studies provide insight into the evolutionary forces facilitating adaptive change in mitochondrial and nuclear OXPHOS genes. iii Co-Authorship " Chapter 2, “Evolutionary Affinity of Billfishes (Xiphidae and Istiophoridae) and Flatfishes (Pleuronectiformes): independent and trans-subordinal origins of endothermy in teleosts”, was co-authored by Dr. Steve Lougheed and Dr. Chris Moyes. Chapter 3, “Evolutionary Origins of Nuclear-Encoded Cytochrome Oxidase Isoforms”, was coauthored by Tika Kocha, Dr. Steve Lougheed and Dr. Chris Moyes. The Thesis was edited by Dr. Steve Lougheed and Dr. Chris Moyes. iv Acknowledgements " I thank my supervisors, Dr. Chris Moyes (I don!t think two people could have been happier than we have been) and Dr. Steve Lougheed (an Eeyore-like presence in the department), for their invaluable support and direction. I also thank my committee members, Dr. Yuxiang Wang and Dr. Vicki Friesen. Thanks to my labmates Mel, Lauren, Rhiannon and co., XXX, Ana and KB. Special thanks to Tika Kocha for her hard work and fish mongering, and to Dr. Chris Lemoine for his guidance. I thank Anthea + family for their support. I also thank NSERC for their support via the Alexander Graham Bell CGS M. " In Memoriam - Speckles, Shaniqua Johnson, The Hypoxic Eight, Auntie Lau, and others we lost along the way. v Table of Contents ! Abstract!!!!!!!!!!! ii Co-Authorship!!!!!!!!!! iv Acknowledgements!!!!!!!!! v Table of Contents!!!!!!!! ! vi List of Tables! ix List of Figures! x List of Abbreviations! xii Chapter 1: General Introduction and Literature Review! 1 1.1 Overview! 1 1.2 Oxidative Metabolism! 1 1.3 Nuclear- and Mitochondrial-encoded OXPHOS Components! 2 1.4 Evolution of Mitochondrial OXPHOS Genes! 3 1.4.1 Mitochondrial-Encoded Cytochrome Oxidase Subunits" 4 1.4.2 High Performance Fishes" 6 1.4.3 Evolution of Cytochrome Oxidase II in Scombroidei" 7 1.4.4 Billfish Phylogeny" 8 1.5 Evolution of Nuclear OXPHOS Genes! 9 1.5.1 Nuclear-Encoded Cytochrome Oxidase Subunits" 10 1.5.2 Whole Genome Duplication Events" 11 1.5.3 Cytochrome Oxidase Isoforms" 11 1.6 General Goals! 12 1.7 References! 14 vi Chapter 2: Evolutionary Affinity of Billfishes (Xiphidae and Istiophoridae) and Flatfishes (Pleuronectiformes): Independent and Trans-Subordinal Origins of Regional Endothermy in Teleosts! 19 2.1 Abstract! 19 2.2 Introduction! 21 2.3 Results! 24 2.3.1 Individual Mitochondrial Loci Datasets" 24 2.3.2 Concatenated Dataset" 24 2.3.3 Nuclear Datasets" 25 2.4 Discussion! 25 2.4.1 Endothermy as a single morphological trait" 26 2.4.2 Relationship between billfishes, carangids and flatfishes" 27 2.5 Materials and Methods! 32 2.5.1 Sample Collection" 32 2.5.2 DNA Isolation" 33 2.5.3 Loci Amplification, Cloning and Sequencing" 33 2.5.4 Phylogenetic Analysis" 34 2.6 Acknowledgements! 36 2.7 References! 37 2.8 Tables! 43 2.9 Figures! 49 Chapter 3: Evolutionary Origins of the Nuclear-Encoded! 63 Cytochrome Oxidase Isoforms! 63 3.1 Abstract! 63 3.2 Introduction! 64 3.3 Results and Discussion! 68 vii 3.3.1 COX IV Isoforms" 69 3.3.2 COX Va Isoforms" 71 3.3.3 COX Vb Isoforms" 72 3.3.4 COX VIa Isoforms" 73 3.3.5 COX VIb Isoforms" 74 3.3.6 COX VIIa Isoforms" 75 3.3.7 COX VIIb Isoforms" 77 3.3.8 COX VIII Isoforms" 77 3.3.9 COX Subunit Stoichiometries" 78 3.3.10 General Conclusions" 79 3.4 Methods! 80 3.4.1 Gene Sequence Retrieval! 80 3.4.2 Bayesian Analyses" 80 3.4.3 dN/dS Ratios" 81 3.4.4 Sample Collection and RNA Purification" 82 3.4.5 RT-PCR Analysis" 83 3.5 References! 85 3.6 Tables! 89 3.7 Figures! 90 Chapter 4: General Discussion! 110 4.1 Evolution of Mitochondrial-Encoded COX Subunits! 110 4.2 Evolution of Nuclear-Encoded COX Subunits! 113 4.3 Conclusions! 115 4.4 References! 117 Appendix! 118 viii List of Tables ! Chapter 2 Table 2.1. Data parameters. 42 Table 2.2. Partitions. 43 Table 2.3. Bayes Factors. 44 Table 2.4 Mitchondrial sequence data. 45 Table 2.5. Primers used for amplification of loci. 46 Chapter 3 Table 3.1. Primers design for nuclear COX isoform amplification in zebrafish. 90 Appendix Table A1. Rate dN/dS ratio test for COX IV isoforms. 111 ! Table A2. Rate dN/dS ratio test for COX Va isoforms.!! 113 ! Table A3. Rate dN/dS ratio test for COX Vb isoforms.!! 113 ! Table A4. Rate dN/dS ratio test for COX VIa isoforms.!! 114 ! Table A5. Rate dN/dS ratio test for COX VIb isoforms.!! 115 ! Table A6. Rate dN/dS ratio test for COX VIIa isoforms.!! 116 ! Table A7. Rate dN/dS ratio test for COX VIIb isoforms.!! 117 ix List of Figures Chapter 2 Figure 2.1. Three phylogenies of scombroids and billfishes.!! ! ! ! 49 Figure 2.2. Bayesian phylogenetic analysis for the Dloop.!!!!! 50 Figure 2.3. Bayesian phylogenetic analysis for 12S. !!!!! 51 Figure 2.4. Bayesian phylogenetic analysis for 16S. !!!!! 52 Figure 2.5. Bayesian phylogenetic analysis for COX I. !!!!! 53 Figure 2.6. Bayesian phylogenetic analysis for COX II.!!!!! 54 Figure 2.7. Bayesian phylogenetic analysis for ATPase 8.!!!!! 55 Figure 2.8. Bayesian phylogenetic analysis for ATPase 6.!!!!! 56 Figure 2.9. Bayesian phylogenetic analysis for COX III.!!!!! 57 Figure 2.10. Bayesian phylogenetic analysis for Cyt B. !!!!! 58 Figure 2.11. Bayesian phylogenetic analysis for the concatenated dataset under the partition strategy with the strongest 2"ln Bayes factor (P1). !!!!!! 59 Figure 2.12. Bayesian phylogenetic analysis of MLL across billfish, carangid, flatfish and scombroid representatives. !!!!!!!!! 60 Figure 2.13.
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