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Assessing Community Dynamics and Colonization Patterns Of University of Vermont ScholarWorks @ UVM Graduate College Dissertations and Theses Dissertations and Theses 2017 Assessing Community Dynamics and Colonization Patterns of Tritatoma dimidiata and Other Biotic Factors Associated with Chagas Disease Prevalence in Central America Lucia Consuelo Orantes University of Vermont Follow this and additional works at: https://scholarworks.uvm.edu/graddis Part of the Genetics and Genomics Commons, and the Public Health Commons Recommended Citation Orantes, Lucia Consuelo, "Assessing Community Dynamics and Colonization Patterns of Tritatoma dimidiata and Other Biotic Factors Associated with Chagas Disease Prevalence in Central America" (2017). Graduate College Dissertations and Theses. 769. https://scholarworks.uvm.edu/graddis/769 This Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks @ UVM. It has been accepted for inclusion in Graduate College Dissertations and Theses by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. ASSESSING COMMUNITY DYNAMICS AND COLONIZATION PATTERNS OF TRIATOMA DIMIDIATA AND OTHER BIOTIC FACTORS ASSOCIATED WITH CHAGAS DISEASE PREVALENCE IN CENTRAL AMERICA A Dissertation Presented by Lucia C. Orantes to The Faculty of the Graduate College of The University of Vermont In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Specializing in Natural Resources October, 2017 Defense Date: April 19, 2017 Dissertation Examination Committee: Kimberly Wallin, Ph.D., Advisor Sara Helms Cahan Ph.D., Advisor Donna Rizzo, Ph.D., Chairperson Leslie Morrissey, Ph.D. Gillian Galford, Ph.D. Cynthia J. Forehand, Ph.D., Dean of the Graduate Colleg ABSTRACT Chagas disease is caused by the parasite Trypanosoma cruzi and transmitted by multiple triatomine vectors across the Americas. In Central America, the predominant vector is Triatoma dimidiata, a highly adaptable and genetically diverse Hemiptera. In this research, we used a novel reduced-representation DNA sequencing approach to discover community dynamics among multiple biotic factors associated with Chagas disease in Central America, and assess the infestation patterns of T. dimidiata after seasonal and chemical disturbances in Jutiapa, Guatemala. For our first study, we used a hierarchical sampling design to obtain multi-species DNA data found in the abdomens of 32 T. dimidiata specimens from Central America. We aimed to understand (1) the prevalence of T. cruzi infection, (2) the population genetics of the vector and parasite, (3) the blood meal history of the vector, and (4) gut microbial diversity. Our results indicated the presence of nine infected vectors harboring two distinct DTUs: TcI and possibly TcIV. We found significant clusters among T. dimidiata populations in countrywide and within-country levels associated with sylvatic ecotopes and diverse domestic genotypes. There was significantly higher bacteria species richness in infected T. dimidiata abdomens than those that were not infected, with further analysis suggesting that gut bacteria diversity relates to both T. cruzi infection and the local environment. We identified vertebrate blood meals from five T. dimidiata abdomens including chicken, dog, duck and human; however, additional detection methods are necessary to confidently identify blood meal sources. In our second study, we analyzed the GBS genotypes of 440 T. dimidiata specimens collected in two towns of Jutiapa, Guatemala. Our aim was to assess (1) the domestic population patterns that aid the recovery of T. dimidiata after an insecticide treatment in El Carrizal and (2) the seasonal changes that regulate the dispersal of the vector in the untreated communities of El Chaperno. Results showed that the insecticide application was effective at reducing the population abundance immediately after the application in El Carrizal; nevertheless, 18-month post- treatment the town-wide infestation and genetic diversity were recovering. Within-house relatedness among specimens recovered 18 months post-treatment, suggesting that the insecticide treatment failed to fully eliminate domiciliated colonies. In contrast, lack of change in abundance or genetic diversity in El Chaperno implied absence of dispersers from sources beyond the town periphery, while evidence of a decrease of relatedness among individuals implied dispersal among houses. After the insecticide treatment in El Carrizal, population reduction led to lack of genetic spatial autocorrelation; nevertheless, rapid dispersal into neighboring houses lead to autocorrelation 18 months after the insecticide treatment. This pattern was also observed in El Chaperno, where an increase in spatial autocorrelation during seasonal dispersal suggests spillover to close-by households. The creation of a novel genomics pipeline allowed us to understand community and dispersal patterns of T. dimidiata and other biotic factors important for the prevalence and transmission of Chagas disease at local and regional levels. Future studies should include complementary approaches for taxa verification (e.g. bacteria 16S barcoding, PCR-base detection), as well as expand the scope of local population analyses to peridomestic and sylvatic genotypes that could suggest a broader range of vector sources and region-wide patterns of temporal and spatial dispersion. CITATIONS Material from this dissertation has been submitted for publication to the Journal of PLOS Neglected Tropical Disease on February 20th, 2017 in the following form: Orantes, L. C. et al. Community Genomics of Chagas Disease: Uncovering vector, parasite, blood meal and microbiome patterns from mixed-DNA specimens of Triatoma dimidiata in Central America. PLOS Neglected Tropical Diseases. ii ACKNOWLEDGEMENTS I would like to thank my advisors, Dr. Kimberly Wallin and Dr. Sara Helms Cahan, for their guidance, support, and encouragement during the entire graduate school process. Thanks to the Chair of my committee, Dr. Donna Rizzo, for all the mentorship and kind advice. Thanks Dr. Leslie Morrissey and to Dr. Gillian Galford for the mentorship and graciously accepting to be part of my committee. Many thanks to my EEID NSF project collaborators, Dr. Carlota Monroy, Dr. Lori Stevens, Dr. Patricia Dorn, Dr. Silvia Justi, Dr. John Hanley, Raquel Lima, Antonieta Rodas, Elizabeth Solórzano, and Gabriela Rodas, for all the help, advice, and resources that have made this research possible. I would also like to thank all the members of the Wallin Lab and the Helms Cahan Lab, past and present, for the moral support and helpful discussions. Thanks to all the students, volunteers, and friends that put many hours of hard work into this project including, Dr. Heather Axen, Dr. Dulce Bustamante, Anthony Nigrelli, Nydiana Benitez, Rachel Frederickson, Laura Haines, Laura Schuster, Sylvia Stevens- Goodnight, Henry Harder, and Lincoln Pierce. Thanks to the Ministry of Health in Guatemala, and CENSALUD in El Salvador for their guidance in the Field, and to the communities that welcomed us into their homes in Guatemala, El Salvador and throughout Central America. Last, I would like to thank my amazing family for being the support system that has carried me through this program. This research was funded by an Ecology and Evolution of Infectious Diseases (EEID) grant from the National Science Foundation (NSF). iii TABLE OF CONTENT CITATIONS ....................................................................................................................... ii ACKNOWLEDGEMENTS ............................................................................................... iii LIST OF TABLES .............................................................................................................. v LIST OF FIGURES ........................................................................................................... vi CHAPTER 1. INTRODUCTION ....................................................................................... 1 1.1. Epidemiology of Chagas Disease .................................................................... 1 1.2. Genetic diversity of T. cruzi and T. dimidiata ................................................. 3 1.3. Life history and population ecology of T. dimidiata ....................................... 4 1.4. Pesticide use to control domestic triatomines .................................................. 6 1.5. Dynamics of bacteria communities in the gut of triatomines .......................... 8 1.6. Overview of reduce representation sequencing techniques ............................. 9 1.7. References ...................................................................................................... 18 CHAPTER 2. COMMUNITY GENOMICS OF CHAGAS DISEASE: UNCOVERING VECTOR, PARASITE, BLOOD MEAL AND MICROBIOME PATTERNS FROM MIXED-DNA SPECIMENS OF TRIATOMA DIMIDIATA IN CENTRAL AMERICA ................................................... 26 2.1. Abstract .......................................................................................................... 27 2.2. Author Summary ............................................................................................ 29 2.3. Introduction .................................................................................................... 30 2.4. Methods.......................................................................................................... 34 2.5. Results ...........................................................................................................
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