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Phylogeny and Molecular Evolution of the Voltage-Gated Sodium Channel Gene Scn4aa in the Electric Fish Genus Gymnotus

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Phylogeny and Molecular Evolution of the Voltage-Gated Sodium Channel Gene Scn4aa in the Electric Fish Genus Gymnotus Phylogeny and Molecular Evolution of the Voltage-Gated Sodium Channel Gene scn4aa in the Electric Fish Genus Gymnotus by Dawn Dong-yi Xiao A thesis submitted in conformity with the requirements for the degree of Masters of Science Cell and Systems Biology University of Toronto © Copyright by Dawn Dong-yi Xiao « 2014 » Phylogeny and Molecular Evolution of the Voltage-Gated Sodium Channel Gene scn4aa in the Electric Fish Genus Gymnotus Dawn Dong-yi Xiao Masters of Science Cell and Systems Biology University of Toronto « 2014 » Abstract Analyses of the evolution and function of voltage-gated sodium channel proteins (Navs) have largely been limited to mutations from individual people with diagnosed neuromuscular disease. This project investigates the carboxyl-terminus of the Nav paralog (locus scn4aa 3’) that is preferentially expressed in electric organs of Neotropical weakly-electric fishes (Order Gymnotiformes). As a model system, I used the genus Gymnotus, a diverse clade of fishes that produce species-specific electric organ discharges (EODs). I clarified evolutionary relationships among Gymnotus species using mitochondrial (cytochrome b, and 16S ribosome) and nuclear (rag2, and scn4aa) gene sequences (3739 nucleotide positions from 28 Gymnotus species). I analyzed the molecular evolution of scn4aa 3’, and detected evidence for positive selection at eight amino acid sites in seven Gymnotus lineages. These eight amino acid sites are located in motifs that may be important for modulation of EOD frequencies. ii Acknowledgments This project would not have been possible were it were not for my supervisor Dr. Nathan Lovejoy, for providing me with the opportunity to work on this project, and giving me the freedom to take initiative. I am thankful for the support of my supervisory committee members, Dr. Asher Cutter, and Dr. Mark Fitzpatrick. I am also indebted to Ian Buglass, for sharing a positive outlook and encouragement. I am grateful for the role that several people played in enhancing the content of my thesis, and the role my supervisor played in facilitating these opportunities. Thanks to Hermina Ghenu, for taking me through my first RNA extraction and cDNA amplification. I might still have your “1 free PCR” coupon among my lab notes somewhere! Thanks to Dr. Belinda Chang, for introducing me to the world of molecular evolution. Thanks to Mu-Quing Huang, not only for providing those gene sequences that I obtained from lab records, but more importantly, for providing additional perspectives on data formatting during the time we worked together. Special thanks to Dr. Ari Chow, who not only shared tips on primer design, but inspired me to cultivate perseverance and uphold scientific integrity. Special thanks to Dr. Shelley Brunt, who not only provided me prompt advice on high throughput PCR techniques, but helped instill critical thinking skills in myself and countless other students. I also wish to thank my family, friends, and colleagues for their continued support, encouragement, and especially for sharing advice from their graduate school experiences. This project was funded by grants awarded to me from the Sigma Xi the Scientific Research Society (Grant-in-Aid of Research, in spring 2009) and the Society of Systematic Biologists (Graduate Student Research Award, in summer 2009). Thank you for taking a chance on me! Funding was also provided through an NSERC discovery grant to Dr. Nathan Lovejoy, and various grants & TA-ships from the University of Toronto. iii Table of Contents Abstract .......................................................................................................................................... ii Acknowledgements ...................................................................................................................... iii Table of Contents ...................................................................................................................... iv-v List of Tables ................................................................................................................................ vi List of Figures .............................................................................................................................. vii List of Appendices .................................................................................................................. viii-ix Chapter 1: Introduction .......................................................................................................... 1-20 1.1 Overview ................................................................................................................................ 1-2 1.2 Clades of Electric Fish ........................................................................................................... 2-3 1.3 Phylogeny, Biogeography, and Morphology of Gymnotiformes .......................................... 4-6 1.4 Phylogeny, Biogeography, and Morphology of Gymnotus ................................................... 6-7 1.5 Evolutionary Adaptations of Electric Organ Discharges in Neotropical American Knifefishes ................................................................................................................................. 8-11 1.6 Anatomy and Neuronal Control of Electric Organs ............................................................... 11 1.7 Cellular Features of Electrocytes and Molecular Basis of Membrane Excitability ........... 12-13 1.8 Genetic Evolution and Protein Expression of Voltage-Gated Sodium Channels ................... 14 1.9 Molecular Features and Mechanisms of Voltage-Gated Sodium Channels ...................... 15-18 1.10 Significance and Objectives ............................................................................................. 18-20 Chapter 2: Materials and Methods ...................................................................................... 21-34 2.1 Taxon Sampling ...................................................................................................................... 21 2.2 Locus Selection .................................................................................................................. 21-22 2.3 Primer Design .................................................................................................................... 22-25 2.3.1 Amplification Primers for scn4aa 3’ .............................................................................................................. 22-25 2.3.2 Sequencing Primers ............................................................................................................................................ 25 iv 2.4 DNA and RNA Extraction ................................................................................................. 25-26 2.5 Nucleotide Amplification and Sequencing ............................................................................. 26 2.6 Nucleotide Sequence Verification and Alignment ............................................................ 26-30 2.7 Phylogenetic Reconstruction ............................................................................................. 30-31 2.8 Molecular Evolution Analyses ........................................................................................... 31-34 Chapter 3: Results .................................................................................................................. 35-52 3.1 Differences Between DNA and cDNA Sequences for the scn4aa 3’ ..................................... 35 3.2 Nucleotide Sequence Data ................................................................................................. 35-36 3.3 Phylogenetic Reconstruction ............................................................................................. 36-41 3.4 Patterns of Gymnotus scn4aa C-terminus Nucleotide Sequence Variation ....................... 41-45 3.5 Positively Selected Sites on the Gymnotus Nav1.4a C-terminus Amino Acid Alignment 46-51 Chapter 4: Discussion ............................................................................................................ 52-60 4.1 Evolutionary Relationships Among Gymnotus .................................................................. 52-53 4.2 Utility of the scn4aa 3’ for Phylogenetic Reconstruction .................................................. 53-54 4.3 Natural Selection at the Nav1.4a C-terminus Among Gymnotus Lineages ....................... 55-56 4.4 Natural Selection at Specific Sites of the Nav1.4a C-terminus Among Gymnotus ............ 57-59 4.5 Summary and Future Directions ........................................................................................ 59-60 References ............................................................................................................................... 61-76 v List of Tables Table 1. Primer Sequences ........................................................................................................... 23 Table 2. cDNA Sequences Used for scn4aa 3’ Primer Design .................................................... 24 Table 3. Specimens and Nucleotide Sequences Used for Gymnotus Analysis ....................... 27-29 Table 4. Models of Evolution Analyzed for the Gymnotus Nav1.4a C-terminus ........................ 33 Table 5. Patterns of Gymnotus Nav1.4a C-terminus Nucleotide Sequence Variation ................. 43 Table 6. Nav1.4a C-terminus ω ratios for Gymnotus from the branch-site model A ................... 45 Table 7. Amino Acid
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