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Evolution of Bat-Trypanosome Associations and the Origins of Chagas Disease

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Evolution of Bat-Trypanosome Associations and the Origins of Chagas Disease City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 2-2015 Evolution of Bat-Trypanosome Associations and the Origins of Chagas Disease Christian Miguel Pinto Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/608 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] Evolution of bat-trypanosome associations and the origins of Chagas Disease By C. Miguel Pinto A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2015 © 2015 C. MIGUEL PINTO All Rights Reserved ii This manuscript has been read and accepted for the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. Susan L. Perkins____________________________________________ ______________________ __________________________________________________________ Date Chair of Examining Committee Laurel Eckhardt_____________________________________________ _______________________ _________________________________________________________ Date Executive Officer Nancy B. Simmons______________________________________________ Michael J. Hickerson_____________________________________________ Stephane Boissinot______________________________________________ Liliana M. Dávalos_______________________________________________ Supervisory Committee THE CITY UNIVERSITY OF NEW YORK iii Abstract EVOLUTION OF BAT-TRYPANOSOME ASSOCIATIONS AND THE ORIGINS OF CHAGAS DISEASE By C. Miguel Pinto Adviser: Doctor Susan L. Perkins Trypanosoma cruzi is a genetically diverse parasite that causes Chagas disease, one of the most important zoonoses in the Americas. This generalist parasite of mammals belongs to a clade mostly comprised of bat parasites, the T. cruzi clade. The origins (i.e., biogeographic history and evolution of hosts associations) of this parasite are far from being understood, and the main areas that need further study are: species limits within T. cruzi sensu lato, further studies on the diversity of T. cruzi clade members and their hosts, and research on adaptations of the hosts to trypanosome infections. In this dissertation I explore these research areas in five core chapters (Ch.2 to Ch.6), and these are the main results per chapter: ch.2) Proposed the recognition of Tcbat as a major diagnostic typing unit of T. cruzi. Ch.3) Found high genetic diversity in the bat exclusive lineage T. c. marinkellei than in the other subdivisions of T. cruzi. Also, reported Tcbat and T. c. marinkellei for Ecuador. Ch.4) Determined that the number of putative species in the T. cruzi clade is underestimated, and more strikingly, that the bat Artibeus jamaicensis is the vertebrate host with the highest number of trypanosomes (5 species) detected in a single locality. Ch.5) Results indicate that T. cruzi sensu lato is actually comprised of three species - the generalist T. cruzi, and two parasites of bats, Trypanosoma marinkellei and Trypanosoma sp. nov.; that there is a previously undetected high diversity of T. cruzi relatives associated with bats, iv and use of bats as hosts has evolved several times and in three different clades of parasites. Ch.6) Tested the hypothesis that immune genes in bats evolve under stronger positive selection than in other mammals because of the high diversity of pathogens associated with bats—including trypanosomes of the T. cruzi clade. I used the gene TLR2, as a candidate gene. These results help to understanding better the diversity of the T. cruzi clade, and the importance of bats on the origins of T. cruzi sensu strict and Chagas disease. v ACKNOWLEDGMENTS I specially thank my partner Verónica Crespo-Pérez for her unconditional support during the last year and half, the hardest and the best of this academic journey. I am very fortunate to have great friends that gave me moral support during my PhD studies, to all of them my most sincere thank you. I am particularly grateful to friends at the following institutions, at AMNH: Robin M. D. Beck, Santiago Claramunt, André Carvalho, Gloria Carvalho, Nadine Duperré, Laureano González-Ruíz, Edmundo González-Santillán, Alejandro Grajales, Camille Grohe, Christine Johnson, Isabelle Kruta, Simone Loss, John Maisey, Aja Marcato, Angelica Menchaca, Alejandro Oceguera-Figueroa, Alan Pradel, Natalia Rossi, Jocelyn Sessa, Angelo Soto-Centeno, Ellen Trimarco, John Wahlert, Eileen Westwig; at CUNY: Elliot Aguilar, JT Boehn, Xin Chen, Terry Demos, Peter Galante, Stephen Harris, Sara Ruane, Mariano Soley, Mark Tollis; at University of Ulm: Gerardo Algara-Siller, Tania González, Tonatiuh Ruíz and Julia Treitler. For facilitating my research, I thank the staff members of the Centro de Investigación en Enfermedades Infecciosas at PUCE, the Sackler Institute for Comparative Genomics, the Laboratory for Conservation Genetics at the National Zoo Park, the Division of Mammals at the Smithsonian Institution, the Department of Mammalogy at the AMNH, the Mammal Collection at the FMNH, the Institute for Experimental Ecology al University of Ulm, Michel Tibayrenc and Jenny Telleria at the IRD-Montpellier, and John Hanson at Research and Testing. Also, I would like to thank the administrative staffs that have helped me along these years with all sorts of paperwork: Mohammad Faiz, Anna Manuel, Sue Ng-Maresco, Joan Reid, María Rios, Elizabeth Sweeny and Eileen Westwig. I thank all my colleagues with whom I have developed these dissertation projects: Elisabeth K. V. Kalko, Iain Cottontail, Nele Wellinghausen,Veronika M. Cottontail, Sofía vi Ocaña-Mayorga, Elicio E. Tapia, Simón E. Lobos, Alejandra P. Zurita, Fernanda Aguirre- Villacís, Amber MacDonald, Anita G. Villacís, Luciana Lima, Marta M. G. Teixeira, Mario J. Grijalva, Susan L Perkins, Marco Tschapka, Kristofer M. Helgen, Bruce D. Patterson, William T. Stanley, Michelle Yu, Burton K. Lim, Jorge Ortega, Carlos A. Flores-López, Carlos A. Machado, Felix Martinez, Craig Willis, DeeAnn M. Reeder, Steven M. Goodman, Robert C. Fleischer, Nancy B. Simmons, and Liliana Davalos. Also, I thank all members of my PhD committee: Susan Perkins, Nancy Simmons, Michael Hickerson, Stephane Boissinot and Liliana Dávalos. This work has benefited from an « Investissements d’Avenir » grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01); a Grant-in-Aid, a Shadle Fellowship and an ASM Graduate Student Fellowship, all from the American Society of Mammalogists; a graduate fellowship from the Smithsonian Institution; an Annette Kade Fellowship and a Graduate Student Fellowship both from the AMNH; A Science Fellowship from CUNY; and NSF-DDIG grant DEB-1311582. vii TABLE OF CONTENTS ABSTRACT………………………………………..…….……………………………………...iv ACKNOWLEDGMENTS……..………………………………………………………………..vi TABLE OF CONTENTS……………………………………………………………...……....viii LIST OF TABLES…………………………………………………………….………………....x LIST OF FIGURES……………………………………………………………...……..…….....xi CHAPTER 1: Introduction—the Trypanosoma cruzi clade and its mammalian hosts ..……1 CHAPTER 2: Tcbat a bat-exclusive lineage of Trypanosoma cruzi in the Panama Canal Zone, with comments on its classification and the use of the 18S rRNA gene for lineage identification …...……………………………………………………………………………….17 CHAPTER 3: Bats, trypanosomes, and triatomines in Ecuador: new insights into the diversity, transmission, and origins of Trypanosoma cruzi and Chagas disease ..………….29 CHAPTER 4: High local diversity of Trypanosoma in a common bat species, and implications for the biogeography and taxonomy of the T. cruzi clade ……………....…….49 CHAPTER 5: Origins of Trypanosoma cruzi and evolution of bat-trypanosome associations ……………...……………………………………………………………………………....…….64 CHAPTER 6: Comparative evolution of the TLR2 gene in bats: effects of phylogeny, life traits and parasite exposure ..…………………………………………………………....…….92 CHAPTER 7: Conclusions and Future Work …………………………………….…..…….118 APPENDIX 3.1.……………………………….………………………….……………………126 APPENDIX 4.1.…………………………………………………………………………..……136 APPENDIX 5.1.…………………………………………………………………………..……141 APPENDIX 5.2.…………………………………………………………………………..……145 viii APPENDIX 6.1.…………………………………………………………………………..……154 APPENDIX 6.2.…………………………………………………………………………..……158 APPENDIX 6.3.…………………………………………………………………………..……159 APPENDIX 6.4.…………………………………………………………………………..……162 APPENDIX 6.5.……………………………………………………………………………..…166 BIBLIOGRAPHY…………..…………………………………………………………………170 ix List of Tables Table 2.1. Mean genetic distances of the 18S rRNA gene, TrN+G model, among Trypanosoma dionisii, T. cruzi marinkellei, T. cruzi DTUs, and TcBat, (below the diagonal), and their standard error estimates (above the diagonal) ...........................................................................................26 Table 3.1. Results of PCR screenings for Trypanosoma cruzi and Trypanosoma rangeli ........42 Table 6.1. ω values of the TLR2 gene for selected braches of the mammalian phylogeny .....106 Table 6.2. Codons of the TLR2 gene under positive selection as estimated by four branch-site methods .....................................................................................................................................107 Table 6.3. Tajima’s D and Pi values for the TLR2 and COI genes
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