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Molecular Phylogenetics of the Rhinoceros Clade And MOLECULAR PHYLOGENETICS OF THE RHINOCEROS CLADE AND EVOLUTION OF UCP1 TRANSCRIPTIONAL REGULATORY ELEMENTS ACROSS THE MAMMALIAN PHYLOGENY By Michael J. Gaudry A Thesis submitted to the Faculty of Graduate Studies of The University of Manitoba In partial fulfillment of the requirements of the degree of MASTER OF SCIENCE Department of Biological Sciences University of Manitoba Winnipeg Canada Copyright © 2017 by Michael J. Gaudry ABSTRACT Aiming to resolve contentious phylogenetic relationships among rhinoceros subfamilies (Dicerorhininae, Rhinocerotinae, and Dicerotinae), I constructed a ~131 kilobase nuclear DNA dataset for the Malayan tapir and six rhinoceros species, including the extinct woolly rhinoceros. Phylogenetic analyses, possibly confounded by incomplete lineage sorting associated with quick ancestral speciation events, yielded opposing trees: ((Dicerorhininae, Rhinocerotinae) Dicerotinae) or (Rhinocerotinae (Dicerorhininae, Dicerotinae)), though five of six informative indels independently supported the latter relationship. Additionally, eye genes revealed no inactivating mutations that may underlie reputedly poor vision among rhinoceroses. Furthermore, I investigated thermogenic UCP1 transcriptional regulators among 139 mammal species, expecting deleterious mutations in eutherians possessing UCP1 pseudogenes and possibly even large-bodied species (e.g. rhinoceroses) that retain intact UCP1. Promoters and enhancers were conserved in all species with intact UCP1, suggesting that it remains functionally expressed in these species. However, these elements have been lost in some UCP1-less species, indicating the enhancer is non-pleotropic. ii ACKNOWLEDGMENTS I would especially like to thank my supervisor, Kevin Campbell, for his endless support over the course of my research. I will be forever appreciative for his advice and willingness to share his vast expertise. His energetic enthusiasm and curiosity have been increadibly motivational and he has shown me what it means to be a scientist. I was also lucky to receive valuable recommendations and guidance throughout my research from my committee members, Jason Treberg and Martin Jastroch. I deeply appreciate the knowledgable suggestions offered by Mark Springer, as well as his generosity in providing DNA samples. I am grateful of Tom Gilbert, Eske Willerslev, and Rasumus Havmøller for suppling Malayan tapir, Sumatran rhinoceros and woolly rhinoceros tissue samples, which were used in the construction of DNA libraries thanks to the hard work of Tony Signore and Nathan Wales. Peter van Coeverden de Groot kindly provided me with extremely rare Javan rhinoceros bone samples. I also thank Margaret Docker for allowing me to use her Ion Torrent sequencer. Kai He took the time to teach me many of the molecular techniques that I utilized during this research, for which I am very grateful. Finally, I would like to express my deep gratitude to my family and friends for always offering their unconditional love and support. This research was funded by a Manitoba Graduate Scholarship, G.A. Lubinsky Memorial Scholarship, an NSERC Discovery Grant, and an NSERC Discovery Accelerator Supplement. iii TABLE OF CONTENTS MOLECULAR PHYLOGENETICS OF THE RHINOCEROS CLADE AND EVOLUTION OF UCP1 TRANSCRIPTIONAL REGULATORY ELEMENTS ACROSS THE MAMMALIAN PHYLOGENY..............................................................i ABSTRACT.......................................................................................................................ii ACKNOWLEDGMENTS................................................................................................iii TABLE OF CONTENTS.................................................................................................iv LIST OF TABLES..........................................................................................................viii LIST OF FIGURES..........................................................................................................ix LIST OF ABBREVIATIONS.........................................................................................xii CHAPTER 1: GENERAL INTRODUCTION................................................................1 CHAPTER 2: MOLECULAR PHYLOGENETICS OF THE RHINOCEROS CLADE.............................................................................................................................10 2.1. Abstract....................................................................................................................... 10 2.2. Introduction................................................................................................................ 11 2.2.1. General introduction.................................................................................... 11 2.2.2. Perissodactyl evolution............................................................................... 12 2.2.3. Rhinoceros evolution.................................................................................. 13 2.2.4. Previous studies of rhinoceros evolution..................................................... 19 2.2.5. Rhinoceros eyesight.................................................................................... 23 2.2.6. Objectives.................................................................................................... 24 2.3. Materials and Methods............................................................................................... 25 2.3.1. Sampling...................................................................................................... 25 iv 2.3.2. Construction of DNA libraries.................................................................... 26 2.3.2.1. Black and Indian rhinoceros DNA library preparation................ 26 2.3.2.2. Javan rhinoceros DNA extraction and library preparation........... 28 2.3.2.3. Malayan tapir and Sumatran rhinoceros DNA extraction and library preparation..................................................................................... 30 2.3.2.4. Woolly rhinoceros DNA extraction and library preparation........ 31 2.3.3. In-solution hybridization captures............................................................... 34 2.3.4. Ion Torrent next-generation sequencing..................................................... 37 2.3.5. Sequenced read assemblies ........................................................................ 39 2.3.6. Genome mining........................................................................................... 40 2.3.7. DNA Alignments........................................................................................ 41 2.3.8. Phylogenetic analyses................................................................................. 41 2.3.8.1. Coalescence analyses................................................................... 41 2.3.8.2. Concatenation analyses................................................................ 43 2.3.8.3. Robinson-Foulds distances.......................................................... 45 2.3.9. Eye gene selection pressure using PAML.................................................. 46 2.4. Results........................................................................................................................ 47 2.4.1. Number of reads sequenced and sequence coverage.................................. 47 2.4.2. Coalescence phylogenetic trees................................................................... 51 2.4.3. Concatenation phylogenetic trees................................................................ 53 2.4.4. Phylogenetically informative indels............................................................ 57 2.4.5. Eye gene selection pressure results............................................................. 58 2.5. Discussion.................................................................................................................. 60 v 2.5.1. Hybridization capture and next-generation sequencing.............................. 60 2.5.2. Rhinoceros phylogenetics........................................................................... 64 2.5.3. Rhinoceros eye gene selection pressure...................................................... 72 2.6. Conclusions................................................................................................................ 73 CHAPTER 3: EVOLUTION OF UCP1 TRANSCRIPTIONAL REGULATORY ELEMENTS ACROSS THE MAMMALIAN PHYLOGENY....................................75 3.1. Abstract...................................................................................................................... 75 3.2. Introduction................................................................................................................ 76 3.2.1. Evolution of uncoupling protein 1............................................................... 76 3.2.2. Evolution of eutherian UCP1 regulatory elements..................................... 83 3.3. Materials and methods............................................................................................... 88 3.3.1. UCP1 regulatory sequences........................................................................ 88 3.3.2. Phylogenetic trees....................................................................................... 93 3.4. Results....................................................................................................................... 94 3.4.1. UCP1 coding sequences.............................................................................
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