Ixodes Scapularis) and Its Host (Peromyscus Leucopus) in Southern Québec
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INTEGRATED LANDSCAPE GENETICS OF THE LYME DISEASE VECTOR (IXODES SCAPULARIS) AND ITS HOST (PEROMYSCUS LEUCOPUS) IN SOUTHERN QUÉBEC by Sarah Sin Tong Leo Department of Biology McGill University, Montreal April, 2016 A thesis submitted to McGill University in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology ©Sarah Sin Tong Leo 2016 For my Family Thank you SUPERVISORY COMMITTEE Dr. Virginie Millien Redpath Museum, McGill University Dr. Andrew Gonzalez Department of Biology, McGill University Dr. Nicholas Ogden Faculté de Médecine Vétérinaire, Université de Montréal Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada Dr. Denis Réale Département de Sciences Biologiques, Université du Québec à Montréal TABLE OF CONTENTS CHAPTER ONE: General Introduction……………….....………………….………………..1 Emerging infectious diseases..............…………………………………………………….1 Emerging vector-borne zoonotic diseases…..…………………………….2 Lyme disease…………………………………………...……………………….…3 Epidemiology…………………………………………………………..….3 The disease-causing organism – Borrelia burgdorferi sensu lato...4 The vector – Ixodes sp. ticks……………………………………..…7 The reservoir hosts and vector hosts……………………………..…10 Lyme disease pathogenesis, diagnosis, and treatment……….…..………13 Pathogenesis………………………………………………………….13 Diagnosis…………………………………………………………..…16 Treatment……………………………………………………………..…17 Lyme disease emergence in Canada and southern Québec…………………………..…18 Role of climate change on Lyme disease emergence in southern Québec…..….19 Role of land use change on Lyme disease emergence in southern Québec……...21 Applying integrated molecular approach in studies on disease emergence dynamic……23 Scope of Thesis……………………………………………………………….……..26 References ……………………………………………………………………………….30 CHAPTER TWO: Multi-taxa integrated landscape genetics for zoonotic infectious diseases: Deciphering variables influencing disease emergence………………….…….……48 Abstract ……………………………………………………………..…………………49 Introduction …………………………………….……………………..…………………50 Material and Methods …………………………………………..………………….……53 Model Overview – Purpose …………………………………………………………….53 Model Overview – Variables and landscapes ……………………………………….53 Model Details – Initialization .………………………...………………………..……. 54 Model Details - Input……………………………………………………………………55 Analysis - Extents, rates, and time taken for disease system emergence……… 56 Analysis - Genetic differentiation among species populations……………………..57 Analysis - Quantifying interspecific interactions facilitating disease emergence.58 Analysis - Landscape features affecting spread…………………………………….. 59 Results …………………………………………………….…………..…………………60 Extents, rates, and time taken for disease system emergence………………………60 Genetic differentiation among species populations….…………………………….61 Quantifying interspecific interactions facilitating disease emergence……………62 Landscape features affecting spread………………………………..…………………62 Discussion…………………………………………………………..………………63 Insights from MTILG on zoonotic infectious disease emergence………………63 Challenges with the framework………………………………...…..…………………65 Applications of the framework ……………………………………..………………… 66 Conclusion…………………………………………………………..………………… 67 References……………………………………………………………..…………………69 Connecting Statement……………………………………………………………………83 CHAPTER THREE: Genetic and morphological variation in white-footed mouse populations at the leading edge of its expanding range: Implications for the emergence of Lyme disease. ...…………………………………………………………………………………84 Abstract ……………………………………………………………..…………………84 Introduction …………………………………….……………………..…………………86 Material and Methods …………………………………………..…………………89 Study sites and specimens …………………………………………………………….89 Microsatellite genotyping………………………………………………..……………..89 Analyses on genetic variation …………………………………………………..……..90 Landscape genetics analyses………………………………………………………….90 Measurements of morphological traits………………………………………………..91 Comparing morphological and genetic variation…………………………………..92 Latitudinal gradients in white-footed mouse morphology and genetics…………..92 Estimating Borrelia burgdorferi presence at site and prevalence in white-footed mice ………………………………………………………………………………………..93 Measures of tick burden on white-footed mouse……………………………………..94 Relations between B. burgdorferi prevalence, tick burden, and mouse genetics and morphology…………………………………………………………………………..94 Results ………………………………………………………………..…………………95 Genetic variation among white-footed mouse populations……………………95 Landscape genetics on white-footed mouse populations …………………………..96 Morphological vs. genetic variation in white-footed mouse……………………..…96 Latitudinal gradients in white-footed mouse morphology and genetics …………97 Borrelia burgdorferi prevalence and black-legged tick burden on white-footed mice………………………………………………………………………………………97 Relations among B. burgdorferi prevalence, tick burdens, and mouse genetics and morphology………………………………………………………………………………98 Discussion……………………………………………………………..…………………98 Genetic variation of white-footed mouse in southern Québec………………99 Morphological variation of white-footed mouse in southern Québec….………101 Role of white-footed mouse on Lyme disease prevalence……..…...…………….102 Conclusion…………………………………………………………..…………………104 References……………………………………………………………..………………105 Connecting Statement…………………………………………………………………118 CHAPTER FOUR: Genetic signature of range expansion in a disease vector and the pattern of Lyme disease emergence…………………………………………………………119 Abstract ……………………………………………………………..…………………119 Introduction …………………………………….……………………..………………120 Material and Methods …………………………………………..…………………122 Study sites and data collection……………………………………………………….122 Genetics analyses………………………………………………….…………………..123 Results ………………………………………………………………..………………125 Spatial genetic patterns in black-legged tick populations………………………125 Spatio-temporal genetic variation in black-legged tick populations….……….125 Status of black-legged tick establishment………………………………………126 Discussion…………………………………………………………..……………127 Employing microsatellites in tick population genetic studies……………………127 Mechanism of black-legged tick range expansion into southern Québec………128 Establishment stages of black-legged tick populations in southern Québec……131 Conclusion…………………………………………………………..…………………132 References…………………………………………………………..…………………134 Connecting Statement…………………………………………………………………147 CHAPTER FIVE: Lyme disease risk from vector and reservoir host species distributions are mediated by climate and landscape heterogeneity……………………………………148 Abstract ……………………………………………………………..…………………148 Introduction …………………………………….……………………..………………149 Material and Methods …………………………………………..………………151 Field data…………………………………………………...…………………………151 Variables influencing Borrelia burgdorferi prevalence……………………………152 Population genetics and multi-taxa integrated landscape genetics on mouse and tick ……………………………………………………………………………………….152 Landscape and habitat effects on mouse density and tick abundance…………153 Climatic variables on mouse and tick occurrence probabilities….………………154 Climate and landscape effect on Lyme disease risk through disease host and vector species……………………………………………………………………………155 Projection of Borrelia burgdorferi prevalence across the study area………….155 Results ………………………………………………………………..………………156 Variables influencing Borrelia burgdorferi prevalence……………………….…156 White-footed mouse and black-legged tick population genetics….…………….156 Landscape and habitat variables on species density and abundance…..……157 Climatic variables on tick and mouse occurrence probabilities………………158 Modeling B. burgdorferi prevalence based on climate and landscape effects on disease host and vector……………………………………………………..………159 Projecting Lyme disease infection risk across the study area……………………159 Discussion…………………………………………………………..………………..…160 Conclusion…………………………………………………………..…………………164 References……………………………………………………………..………………165 CHAPTER SIX: General Conclusions ………………………………….……..……………181 Thesis Summary………………………….……………………………………………181 Future Work …………………………………………………………………..………..184 References………………..……………………………………..………………………186 Appendix A …..……………………….......………………...………………………..………191 Appendix B …………………….......………………...…………………………..………….195 Appendix C …………………….......………………...…………………………..………….202 Appendix D …………………….......………………...…………………………..………….208 LIST OF TABLES Table 2.1. Description of simulated scenarios A to H, with details on the different landscape characteristics (heterogeneity and barriers) and disease dispersal patterns employed in each scenario. The numbers in subscript following Ps and Vs indicate which host species their dispersal is dependent on. Short-distance and long-distance dispersal are driven by H1 and H2, respectively. …………………………………………………………..……………………..…76 Table 2.2. Summary of results from Procrustes rotation tests that determined strength and significance of correlation between interspecific spatial genetic patterns. Associated species refer to pathogen, vector, and host species that were assigned shared spatial dependence and dispersal rates in each scenario. Average correlation coefficients and standard deviations calculated from all replicates are provided. The frequencies of statistically significant correlations are also included in the table. Simulation scenarios are labelled as in Table 2.1. ……..……..………...77 Table 3.1. Summary of results from performing ANOVA on redundancy analyses (RDA) investigating the influence of spatial heterogeneity on white-footed mouse genetic variation. Connectivity among sites was estimated from resistance values