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Evolutionary History and Whole Genome Sequence of Pejerrey (Odontesthes Bonariensis): New Insights Into Sex Determination in Fishes

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Evolutionary History and Whole Genome Sequence of Pejerrey (Odontesthes Bonariensis): New Insights Into Sex Determination in Fishes Evolutionary History and Whole Genome Sequence of Pejerrey (Odontesthes bonariensis): New Insights into Sex Determination in Fishes by Daniela Campanella B.Sc. in Biology, July 2009, Universidad Nacional de La Plata, Argentina A Dissertation submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy January 31, 2015 Dissertation co-directed by Guillermo Ortí Louis Weintraub Professor of Biology Elisabet Caler Program Director at National Heart, Lung and Blood Institute, NIH The Columbian College of Arts and Sciences of The George Washington University certifies that Daniela Campanella has passed the Final Examination for the degree of Doctor of Philosophy as of December 12th, 2014. This is the final and approved form of the dissertation. Evolutionary History and Whole Genome Sequence of Pejerrey (Odontesthes bonariensis): New Insights into Sex Determination in Fishes Daniela Campanella Dissertation Research Committee: Guillermo Ortí, Louis Weintraub Professor of Biology, Dissertation Co-Director Elisabet Caler, Program Director at National Heart, Lung and Blood Institute, NIH, Dissertation Co-Director Hernán Lorenzi, Assistant Professor in Bioinformatics Department, J. Craig Venter Institute Rockville Maryland, Committee Member Jeremy Goecks, Assistant Professor of Computational Biology, Committee Member ! ""! ! Copyright 2015 by Daniela Campanella All rights reserved ! """! Dedication The author wishes to dedicate this dissertation to: My love, Ford, for his unconditional support and inspiration. For teaching me that admiration towards each other’s work is the fundamental fuel to go anywhere. My family and friends, for being there, meaning “there” everywhere and whenever. My grandpa Hugo, a pejerrey lover who knew how to fish, cook and enjoy the “silver arrows”. I was never a good fishing partner, but at least I caught a pejerrey genome! ! "#! Acknowledgements The author wishes to say thank you to: My co-advisor Lis. You were not only an incredible advisor and mentor, but also a friend. Thank you, Emmanuel & Mila for providing me of a home away from home. My co-advisor Guillermo. for giving me the opportunity to move forward in my career, for your guidance, enthusiasm and kind words during tough times. To Hernán, for taking over and guiding me through the bioinformatics jungle. For patiently responding to my hundreds of emails with silly questions. Thank you! To my lab-mates, Lily Hughes, Andrew Thompson, Kerry Mullaney, Roberto “tito” Cifuentes, Ricardo R-Betancur, Dahiana Arcila and Eva Rueda, for teaching me about PCR, fishes and life as a graduate student. Some of you only stayed for a while but made a big difference, and taught me so much. Thank you. Students, friends (Sanghi, Thiago, Chuy, Joey, Cristina), staff, and faculty from the GWU Biology Department, thank you all. To Juani Fernandino & Gustavo Somoza from IIB-INTECH, Chascomús. For sharing your pejerrey knowledge with me, for the countless hours of interesting conversations and the inspiration to explore. To G. Allen, R. Cifuentes, V. Cussac, A. Gosztonyi, J. Graf, E. Habit, G. Lange, M. Loureiro, D. Lumbantobing, A. Saunders, L. Smith, J. Sparks and the many additional people who assisted with collecting, curating, and providing the specimens for the Chapter 2 study. To K. Mullaney for helping with DNA amplifications, and ! #! paleontologist M. E. Raffi who contributed with observations on argentine fossils. To R. Betancur-R who helped with data analysis. To the US National Science Foundation for providing grants DEB 0918073 (to Kyle R. Piller, co-author of Chapter 2), DEB-1019308 and OISE-0530267 (to Guillermo Ortí, co- author of Chapter 2). To The George Washington University, for funding part of my work through the Weintraub Fellowship, Harlan funds, and startup funds to my co-advisor Guillermo Ortí. To the J. Craig Venter Institute in Rockville, Maryland for providing the computational resources, training and fellowship. ! #"! Abstract of Dissertation Evolutionary History and Whole Genome Sequence of Pejerrey (Odontesthes bonariensis): New Insights into Sex Determination in Fishes Recent reduction in the cost of DNA sequencing has enabled unprecedented opportunities to obtain genomic resources for non-model organisms. The main product of this dissertation is the whole-genome sequence of the pejerrey, Odontesthes bonariensis (Atherinopsidae, Atheriniformes, Teleostei), a freshwater species with high value for aquaculture and recreational fisheries and an emerging model system to study the evolution of sex determination in vertebrates. Genomic resources have the potential to quickly expand scientific knowledge by providing direct access to big genetic datasets. This dissertation introduces the first version of the pejerrey genome assembly and annotation based on a shotgun sequencing approach using the Illumina platform of three genomic libraries with different insert sizes. The pejerrey is one of the few fish species known to undergo temperature-dependent sex determination (TSD). Although a major sex-determining gene has been identified recently in several species of Odontesthes, the temperature at which pejerrey eggs or larvae are exposed to during the first weeks of life is a major factor determining phenotypic sex, overriding the effect of the genotype. A direct application of the newly assembled and annotated pejerrey genome provides insight into the regulatory network affecting TSD in fishes. This study reveals potential mechanisms to explain how genetic, environmental, and chemical factors interact in a sex- determining network during key developmental stages of pejerrey. A new perspective is presented on the role of steroid hormones affecting expression of a conserved genetic toolkit shared by species with different sex determination systems. ! #""! To enhance the comparative value of the new genomic resources and place the pejerrey in a well- resolved phylogenetic context, this dissertation provides a new phylogenetic hypothesis based on analyses of new sequence data collected for eight molecular markers for a representative sample of 103 atheriniform species, covering 2/3 of the genera in this order. The new phylogenetic hypothesis is used to recommend some changes in the current classification and is calibrated with six carefully chosen fossil taxa to provide an explicit timeframe for the diversification of this group. Ancestral habitat reconstructions are inferred to test biogeographic hypotheses to explain current distribution of marine and freshwater taxa. Post-Gondwanan divergence times among families are consistent with extensive marine dispersal along the margins of continents with repeated invasion of freshwater habitats. ! #"""! Table of Contents Dedication ..........................................................................................................................iv Acknowledgements .............................................................................................................v Abstract of Dissertation.....................................................................................................vii List of Figures ....................................................................................................................xi List of Tables....................................................................................................................xiii Chapter 1: Introduction and Overview...........................................................................1-23 References.................................................................................................................................. 16 Chapter 2: Multi-locus fossil calibrated phylogeny of Atheriniformes .......................24-70 Introduction................................................................................................................................ 24 Materials & Methods ................................................................................................................. 32 Results........................................................................................................................................ 39 Discussion.................................................................................................................................. 54 References.................................................................................................................................. 64 Chapter 3: The draft genome of Odontesthes bonariensis .........................................71-127 Introduction................................................................................................................................ 71 Materials & Methods ................................................................................................................. 73 Results........................................................................................................................................ 83 Discussion and Conclusions .................................................................................................... 111 References................................................................................................................................ 120 Chapter 4: The draft genome of Odontesthes bonariensis .......................................128-168 ! "$! Introduction.............................................................................................................................
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