Reassessing Colugo Phylogeny, Taxonomy, and Biogeography
Total Page：16
File Type：pdf, Size：1020Kb
REASSESSING COLUGO PHYLOGENY, TAXONOMY, AND BIOGEOGRAPHY BY GENOME WIDE COMPARISONS AND DNA CAPTURE HYBRIDIZATION FROM MUSEUM SPECIMENS A Dissertation by VICTOR CHRISTIAN MASON Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, William J Murphy Committee Members, Kristofer M Helgen Paul Samollow Tiffani Williams James Cai Head of Department, Dorothy Shippen May 2016 Major Subject: Genetics Copyright 2016 Victor Christian Mason ABSTRACT The ability to uncover the phylogenetic history of archived museum material with molecular techniques has rapidly improved due to the reduced cost and increased sequence capacity of next-generation sequencing technologies. However it remains difficult to isolate large, orthologous DNA regions across multiple divergent species. Here we describe the use of cross-species DNA capture hybridization techniques and next-generation sequencing to selectively isolate and sequence mitochondrial DNA genomes and nuclear DNA from the degraded DNA of museum specimens, using probes generated from the DNA of an extant species. Colugos are among the most poorly understood of all living mammals despite their central role in our understanding of higher-level primate relationships. Two described species of these extreme gliders are the sole living members of a unique mammalian order, Dermoptera, distributed throughout Southeast Asia. We generated a draft genome sequence for a Sunda colugo and a reference alignment for the Philippine colugo, and used these to identify colugo-specific enrichment in sensory and musculo- skeletal related genes that likely underlie their nocturnal and gliding adaptations. Phylogenomic analysis and catalogs of rare genomic changes overwhelmingly support the hypothesis that colugos are the sister group to primates (Primatomorpha), to the exclusion of treeshrews. We also captured ~140-kb of orthologous sequence data from colugo museum specimens sampled across their range, and identified deep genetic structure between many geographically isolated populations of the two named species, ii consistent with a remarkable increase in diversity. Our results identify conservation units to mitigate future losses of this enigmatic mammalian order. Examining multiple distantly related mammals we identified a consistent pattern of early diversification between east and west Borneo including colugos, the lesser mouse deer, and pangolins. This strongly parallel biogeographic pattern is not common in mammals and we see no evidence for this pattern in the greater mouse deer. Colugos on West Borneo diverged from those in Indochina in the late Pliocene, however most other mammals across this same geographic region diverged from their common ancestor much more recently in the Pleistocene. Low genetic divergence between colugos on large landmasses and colugos on neighboring islands indicate that past forest distributions in the recent past were recently much larger than present refugial distributions. iii ACKNOWLEDGEMENTS I want to start off by thanking my PI, committee chair, and friend Dr. William Murphy for not only giving me an opportunity to pursue my scientific interests, but also for being the best role-model a student could ask for. He has pushed me to strive for goals I assumed to be out of reach, and has always been available and happy to discuss my sometimes rather ridiculous ideas. Dr. Murphy has always put the well-being of his students first and given myself and others substantial scientific and personal opportunities to develop and grow to be better people. I attribute a large part of what I have achieved and what I want to achieve to him alone. I would like to thank Dr. Kristofer Helgen for being exceptionally positive, and an enormous facilitator of this dissertation. He traveled around the world with me to sample museum specimens and measure hundreds of colugo skulls used for this dissertation. In addition, his truly encyclopedic knowledge of mammals has generated integral intellectual contributions to our hypotheses and conclusions. I would like to thank my committee member Dr. Paul Samollow for taking the time to critically think and comment on my dissertation. Dr. Samollow has always understood the true meaning of things. He always has something insightful and uplifting to say and I value all of our conversations. My interactions with both Dr. Murphy and Dr Samollow as an undergraduate student convinced me to pursue a doctoral degree. I also want to thank my committee member Dr. Tiffani Williams for introducing me to Python which allowed me to apply my own ideas to big data, and for reminding iv me that reproducibile results are the only real scientific results. Thank you to my committee member Dr. James Cai for broadening my bioinformatic knowledge and being a part of this entire journey. Thank you to everyone that has been a part of the Murphy lab over the years, Particularly Dr. Gang Li, Dr. Brian Davis, and M.S. Wesley Brashear. Dr. Li has answered so many of my questions over the years, and been a great friend. Thanks Wesley for being a backboard that I can bounce ideas off of at any moment and being an exceptional friend. Graduate school has been difficult at times, and my family has stood beside me through everything, my parents Jacque and Richard Mason and, my brothers Austin and Owen Mason. Of course all of my friends and people close to me throughout graduate school have encouraged me, humbled me, and heavily influenced how I see the world. You know who you are and thank you. Also thank you to the Texas A&M University (TAMU) College of Veterinary Medicine, TAMU Institute for Genome Sciences and Society, the TAMU Genetics Graduate Student Association, the National Human Genome Research Institute (NHGRI), and the National Science Foundation (NSF) for funding various aspects of this project. v TABLE OF CONTENTS Page ABSTRACT……………………………………………………………………………...ii ACKNOWLEDGEMENTS ...………………………………………...…………………iv TABLE OF CONTENTS……………………………………….……………………….vi LIST OF FIGURES…………………………………………………………………….viii LIST OF TABLES………………………………………………………………………..x CHAPTER I INTRODUCTION AND LITERATURE REVIEW ...…………………….1 1.1 Colugos ............................................................................................................. 1 1.2 Current and Historical Taxonomy of Dermoptera ........................................... 4 1.3 Historical Interordinal Relationships of Dermoptera ....................................... 7 1.4 Biogeography ................................................................................................... 9 1.5 Application of Capture Hybridization Techniques to Museum Specimens ... 12 1.6 Aims and Structure of the Dissertation .......................................................... 13 CHAPTER II EFFICIENT CROSS-SPECIES CAPTURE HYBRIDIZATION AND NEXT-GENERATION SEQUENCING OF MITOCHONDRIAL GENOMES FROM NON-INVASIVELY SAMPLED MUSEUM SPECIMENS .......................................... 15 2.1 Introduction .................................................................................................... 15 2.2 Results ............................................................................................................ 19 2.3 Discussion ...................................................................................................... 31 2.4 Methods .......................................................................................................... 38 2.5 Data Access .................................................................................................... 45 CHAPTER III GENOMIC ANALYSIS REVEALS REMARKABLE HIDDEN BIODIVERSITY WITHIN COLUGOS AND THE SISTER GROUP TO PRIMATES 46 3.1 Introduction .................................................................................................... 46 3.2 Results and Discussion ................................................................................... 48 vi 3.3 Methods .......................................................................................................... 61 CHAPTER IV COLUGO BIOGEOGRAPHY REVEALS PALEO-FOREST CORRIDORS THROUGHOUT SUNDALAND ............................................................ 88 4.1 Introduction .................................................................................................... 88 4.2 Materials and Methods ................................................................................... 94 4.3 Results .......................................................................................................... 101 4.4 Discussion .................................................................................................... 106 4.5 Conclusions and Future Research ................................................................ 117 CHAPTER V CONCLUSIONS ..................................................................................... 119 5.1 DNA Capture Hyrbidization ........................................................................ 119 5.2 Divergence Dating ........................................................................................ 120 5.3 Phylogeography ............................................................................................ 121 5.4 Future Directions .......................................................................................... 123 5.5 Recommended Taxonomic Revisions .......................................................... 124