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The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes

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The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes. by Andrew William Thompson B.S. in Biology, December 2009, Clarion University of Pennsylvania 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, 2017 Guillermo Ortí Louis Weintraub Professor of Biological Sciences The Columbian College of Arts and Sciences of The George Washington University certifies that Andrew William Thompson has passed the Final Examination for the degree of Doctor of Philosophy as of August 1, 2016. This is the final and approved form of the dissertation. The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes. Andrew William Thompson Dissertation Research Committee: Guillermo Ortí, Louis Weintraub Professor of Biological Sciences, Dissertation Director. Jason E. Podrabsky, Professor and Chair, Department of Biology, Portland State University, Committee Member. Jeremy Goecks, Assistant Professor of Computational Biology, Committee Member. ii Copyright 2016 by Andrew William Thompson All rights reserved iii Dedication To Jacqueline for being my compass needle towards adventure and my infinite source of strength. To Rian for being my partner in crime. To Mom for encouraging me to always dream bigger. To Dad for showing me that nature is beautiful. To Grandma for our trips to the creek. To Pap for his faith in me. To Uncle Jeff for showing me the honor in hard work. To Aunt Pam for teaching me that science is cool. To Uncle Michael for always finding me when I am away from home. To John and Kate for welcoming me into their family. To Aunt Barb for teaching me that kindness is everything. iv Acknowledgements I have had an incredible amount of support along my way. I thank Andrew Turner at Clarion University for realizing my passion as a freshman and getting me an early start in research. His guidance and mentorship helped paved my way to a Ph.D. I thank all of my friends and colleagues at George Washington University especially Jesus “Chuy” Ballesteros and my labmates Lily Hughes, Daniela Campanella, and Dahiana Arcila for their constant support. Thanks to Robert Kallal, Thiago Moreira, Diana Lipscomb and Gustavo Hormiga for all of their help with the electron microscope. I thank Cori Stone, Anais Hayes, and Kerry Mullaney for all of their help in the laboratory. I am grateful for the mentorship of Ricardo Betancur that was immensely important during that first year of graduate school. I am grateful for the kindness and expertise of Jason Podrabsky, Claire Riggs, and Amie Romney as they welcomed me into their lab and showed me the ways of the killifish. Many thanks to Andrew Furness for donating tissues and specimens. I thank my friends in Brazil for a wonderful collection trip and making me feel at home in a foreign country: Claudio Olivera, Ricardo Britzke, and Jefferson Henriques. I am indebted to my thesis committee members Lynne Parenti, Keith Crandall, and Jeremy Goecks for their guidance. I thank Berkeley Davenport at Children’s National Medical Center for all of his help with sequencing. I thank my wife Jacqueline for all of her help with killifish husbandry. Lastly, I thank my advisor Guillermo Ortí for his confidence in my abilities and his willingness to take on such a different and novel project. I have learned an incredible amount under his leadership. v Abstract of Dissertation The Evolution of Chorionic Ultrastructure, Delayed Hatching, and Desiccation Tolerance in Annual Killifishes Fishes are the most diverse vertebrates on the planet with over 33,000 species. They have colonized every major body of water from caves, toxic environments, the deepest oceans, to temporary pools. Some species in these extreme environments belong to a group of fishes known as killifishes (Cyprinodontiformes: Aplocheiloidei). Often popular pets, killifishes contain over 700 species. These small, colorful fish can be found in habitats inhospitable to all other species of fishes. Killifishes inhabit seasonal pools that dry up, resulting in the death of all adults in the pond. The population is able to survive dry periods as embryos with specialized egg envelopes, unique diapause stages, and desiccation tolerance. We use an integrative approach of scanning electron microscopy (SEM), comparative transcriptomics, and phylogenomics to investigate the evolutionary patterns and genetic processes that led to the evolution of this remarkable trait. We present new data and inferences on egg structure of multiple lineages, hundreds of candidate genes involved diapause and desiccation tolerance, as well as a robust phylogenomic hypothesis for Aplocheiloidei. Specifically, we document egg structure in 52 aplocheiloid species for the first time with SEM. We examine the convergence/parallelism of egg structural characters in a phylogenetic framework. In addition, we use whole transcriptomes to study the evolution of annualism in Aplocheiloidei. Specifically, we find evidence of transcriptional convergence in dormancy across metazoa after identifying significantly differentially expressed transcripts during diapause in the annual killifish Nematolebias whitei. We also identify vi differentially expressed genes during delayed hatching and desiccation tolerance in the non-annual killifish Aplocheilus lineatus providing evidence that delayed hatching is not a form of dormancy. Lastly, we construct a species tree of Aplocheiloidei with 8,000 orthologous loci and verify the convergent/parallel evolution of annualism with “big data.” vii Table of Contents Dedication ..................................................................................................................... iv Acknowledgments .......................................................................................................... v Abstract of Dissertation ................................................................................................ vi List of Figures ............................................................................................................... ix List of Tables ................................................................................................................. x Chapter 1 ........................................................................................................................ 1 Chapter 2 ........................................................................................................................ 9 Chapter 3 ..................................................................................................................... 34 Chapter 4 ...................................................................................................................... 46 Chapter 5 ...................................................................................................................... 68 References .................................................................................................................... 85 viii List of Figures Figure 1.1 ....................................................................................................................... 2 Figure 1.2 ....................................................................................................................... 3 Figure 2.1 ..................................................................................................................... 11 Figure 2.2 ..................................................................................................................... 19 Figure 2.3 ..................................................................................................................... 20 Figure 2.4 ..................................................................................................................... 21 Figure 2.5 ..................................................................................................................... 22 Figure 2.6 ..................................................................................................................... 26 Figure 2.7 ..................................................................................................................... 27 Figure 3.1 ..................................................................................................................... 37 Figure 3.2 ..................................................................................................................... 40 Figure 4.1 ..................................................................................................................... 54 Figure 4.2 ..................................................................................................................... 58 Figure 5.1 ..................................................................................................................... 71 Figure 5.2 ..................................................................................................................... 79 Figure 5.3 ..................................................................................................................... 84 ix List of Tables Table 2.1 ....................................................................................................................... 16 Table 2.2 ......................................................................................................................
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