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Molecular Evolution and Population Genetics of Infectious Diseases Molecular Evolution and Population Genetics of Infectious Diseases By Eduardo Felipe Castro Nallar B.S. in Biochemistry, December 2007, Universidad de Santiago de Chile 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 directed by Keith Alan Crandall Professor of Biological Sciences The Columbian College of Arts and Sciences of The George Washington University certifies that Eduardo Felipe Castro Nallar has passed the Final Examination for the degree of Doctor of Philosophy as of September 16, 2014. This is the final and approved form of the dissertation. Molecular Evolution and Population Genetics of Infectious Diseases Eduardo Felipe Castro Nallar Dissertation Research Committee: Keith A. Crandall, Professor of Biological Sciences, Dissertation Director Amy E. Zanne, Associate Professor of Biological Sciences, Committee Member Guillermo Ortí, Louis Weintraub Professor of Biological Sciences, Committee Member ii Dedication To Romina, the love of my life To my parents, Pablo and Isabel, who taught me to focus, think, and understand the world To René and Paula, for being the most kind and generous siblings an older brother can have To Andrea, for helping me get through my first challenges in research To my friends, for making me company, making me part of something, and making me a better person “Historia magistra vitae et testis temporum” Marcus Tullius Cicero “América, […] vivo en la sombra que me determina, duermo y despierto en tu esencial aurora […]” Pablo Neruda, Canto General, XVIII “You may have noticed that the less I know about a subject the more confidence I have, and the more new light I throw on it” Mark Twain iii Acknowledgements The author wishes to thank the many persons that have been related, at different levels, in the development of this work. First, I would like to thank my wife Romina for her unconditional support during my PhD program. She has been with me every step of the way, always encouraging me to work hard and enjoy what I do. Romi, I could not have done this without you, and I thank you not only for being here with me but also for being my friend. Neither this work nor the person who I am today could exist without the countless opportunities and lessons Keith has always generously provided. I do not recall a single time you have refused any of my whims, from buying fancy computers and books to encouraging me to go to workshops and supporting any research idea that has come to my mind. I still remember that it took me about a day to write an email to you back in 2008 asking you if I could join your lab, and took only a few minutes to get an email back from you saying that you will be glad to receive me. For all that and for being a friend, I thank you. Two institutions and two places shaped my experience as a graduate student. I would like to thank my friends in Utah, especially Arley and Melody that helped me get settled and with which I share so many good moments. I would like to thank Jack Sites, Fernanda, Rafael, César, Ana, and Patri for all the guidance and experiences we shared together. Special thanks go to my friends Justin and Flor (and baby Ben Bagley) that always have been there for me. Thanks to Andrés, Los Vega, Miguel, el primo, Gonzalo and the rest of the crew for giving me my social life back. I would also like to thank the people of the CBI, especially Chris, Sarah, and iv Veronica. I enjoy all our conversations from discussing the weather to the latest TV show to more serious stuff like baseball and basketball games. To Marcos, with which I have learned quickly to be cautious and to think more than twice when I analyze data. I would never be able to keep pace with you in our weekend hikes on the Appalachians but do know that I enjoy them very much. I am also grateful of Guillermo, the Ortí Lab, Amy and the rest of my committee, who have helped me in the lab and advised me during my last two years of program. I would like to thank my undergraduate advisor Eugenio Spencer and my former boss Ana María Sandino for opening my mind to the world with new perspectives and stories, and for believing in me and encouraging me to pursue a PhD abroad. With them I am in debt. Finally, I would like to thank my family and friends in Chile. There are too many to thank here but they know I love them and care for them deeply. Thanks to my mom, Isabel, for teaching me the love of reading and for always making me look for answers in the dictionary and our encyclopedia, for instilling me with hunger to learn always more, and for being with me unconditionally always. Thanks to my dad, Pablo, that in his own way taught me so many essential lessons. I will always admire you. Thanks to my sister Paula, that recently graduated and beat me for a few months. You are the living example that hard work pays off. To René, my little brother that is now a man, thanks for bringing joy, good will, and exceptional stories. Sergio, I followed your advice, I kept my eyes opened, sharpened my senses, and saved only what it was valuable. v Abstract of Dissertation Molecular Evolution and Population Genetics of Infectious Diseases The rapid emergence and spread of infections and the rapid evolution of established pathogens affect our ability to monitor and control disease. Continually, we are reminded of the challenges of controlling disease, not only of pathogens affecting human health, but also those indirectly affecting human activities such as food production. Phylogenetic coalescent methods are conventionally used to infer evolutionary relationships and processes from patterns of homologous characters including genomic data. Viral and bacterial pathogens are especially fit for such inferences, as opposed to in phylogenetic systematics, due to their short generation times, large population sizes, and high substitution rates. These traits enable us to observe changes at the genomic level that are causally linked or correlated to ecological and evolutionary processes. Traditionally, phylogenetic methods, typically used by systematists, have been co-opted and applied to human-related pathogens of health importance; however, little has been done regarding pathogens that affect food production and/or public safety. This work aimed to review the breadth of phylogenetic applications to microorganisms, particularly viruses; and to apply these methods to questions about molecular evolution and population genetics of non-model microorganisms. The first section reviews phylogenetic approaches applied to the study of the model organism Human Immunodeficiency Virus (HIV). I review applications to viral origin, global dispersal, and population genetics of within- and among-host infections. vi The second section deals with relative performance of multi locus sequence typing (MLST) in molecular epidemiology, and whether different molecular survey approaches, namely MLST, single nucleotide polymorphisms, and/or genomes yield comparable inferences regarding origin and dispersal of select agents. Lastly, the third section shows two case studies: a disease outbreak investigation of Infectious Salmon Anemia Virus (ISAV) in Chile with negative consequences to salmon farming, and a Lactococcus phage investigation to understand transmission between affected cheese factories in Australia. In aggregate, this body of work demonstrates the challenges and benefits of using phylogenetic methods to study the evolution of infectious diseases. vii Dissertation citations The following work has been published in scientific journals and below I provide the citations to the fully formatted articles. 1. Castro-Nallar, Eduardo, Marcos Pérez-Losada, Gregory F. Burton, and Keith A. Crandall. "The evolution of HIV: inferences using phylogenetics." Molecular phylogenetics and evolution 62, no. 2 (2012): 777-792. 2. Castro-Nallar, Eduardo, Keith A. Crandall, and Marcos Pérez-Losada. "Genetic diversity and molecular epidemiology of HIV transmission." Future Virology 7, no. 3 (2012): 239-252. 3. Pérez-Losada, Marcos, Patricia Cabezas, Eduardo Castro-Nallar, and Keith A. Crandall. "Pathogen typing in the genomics era: MLST and the future of molecular epidemiology." Infection, Genetics and Evolution 16 (2013): 38-53. 4. Eduardo Castro-Nallar, Nur Hasan, Richard Robison, Rita Colwell, W. Evan Johnson, and Keith A. Crandall. 2014. “Evaluation of genomic tools for molecular epidemiology.” PeerJ 5. Castro-Nallar, Eduardo, Marcelo Cortez-San Martín, Carolina Mascayano, Cristian Molina, and Keith A. Crandall. "Molecular phylodynamics and protein modeling of infectious salmon anemia virus (ISAV)." BMC evolutionary biology 11, no. 1 (2011): 349. 6. Castro-Nallar, Eduardo, Honglei Chen, Simon Gladman, Sean C. Moore, Torsten Seemann, Ian B. Powell, Alan Hillier, Keith A. Crandall, and P. Scott Chandry. "Population genomics and phylogeography of an Australian dairy factory derived lytic bacteriophage." Genome biology and evolution 4, no. 3 (2012): 382-393. viii Table of Contents Dedication .......................................................................................................................... iii Acknowledgements ............................................................................................................ iv Abstract of Dissertation .................................................................................................... vi Dissertation citations
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