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Thesis Submitted for the Degree of Doctor of Philosophy University of Bath PHD Population biology of Ixodes ticks Seelig, Frederik Award date: 2011 Awarding institution: University of Bath Link to publication Alternative formats If you require this document in an alternative format, please contact: [email protected] General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal ? Take down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Download date: 27. Sep. 2021 Population biology of Ixodes ticks By Frederik Seelig A thesis submitted for the degree of Doctor of Philosophy University of Bath Department of Biology and Biochemistry September 2011 COPYRIGHT Attention is drawn to the fact that copyright of this thesis rests with its author. A copy of this thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and they must not copy it or use material from it except as permitted by law or with the consent of the author. This thesis may be made available for consultation within the University Library and may be photocopied or lent to other libraries for the purposes of consultation. Author Signature ……………………………… "Science is the knowledge of consequences, and dependence of one fact upon another." — Thomas Hobbes, Leviathan. "'Is it about a bicycle?', he asked." — Flann O'Brien, The third policeman. Acknowledgements Acknowledgements First and foremost I would like to thank my late supervisor Klaus Kurtenbach, whose knowledge and enthusiasm about ticks, and about sharks, was truly infectious, and who is still dearly missed. This work would not have been possible to complete without the outstanding support that I received from Dr Gabi Margos and Professor Stuart Reynolds. They guided me through my PhD project as the best supervisors one could ask for. I am also most grateful to Dr Ed Feil, who made crucial suggestions about my work on tick endosymbionts, and who put up with my ignorance in phylogenetic matters. My friends and colleagues Stephanie Vollmer and Ruth Dinnis shared many hours of tick collecting, tick crushing, and tick sequence editing, which made these tasks far more entertaining than if I had been on my own. Dr Richard Birtles and Dr Kevin Bown were immensely helpful in establishing the blood meal analysis scheme in our lab, and provided ample suggestions and materials. Dr Nick Waterfield kindly agreed to let me use his clean room facilities for my experiments on borrelia. Stavros Gavkalias performed most of the PCR screening and amplification of Midichloria samples, which contributed greatly to the chapter on tick endosymbionts. Several members of the tick research community made very useful suggestions and offered kind words of encouragement, especially Sarah Randolph, Jean Tsao, Joe Piesman, and Reuben Kaufman. The members of my lab are to be thanked for giving helpful advice, having lunch breaks by the lake, and sharing my belief in a life outside the laboratory. My wonderful family encouraged and supported me through my entire studies in every possible way. Finally, I would like to thank Sara for being my North, South, East, and West whenever I lost my compass. iii Publications Publications • Host migration impacts on the phylogeography of Lyme Borreliosis spirochaete species in Europe. (2011). Stephanie A. Vollmer, Antra Bormane, Ruth E. Dinnis, Frederik Seelig, Andrew D.M. Dobson, David M. Aanensen, Marianne C. James, Michael Donaghy, Sarah E. Randolph, Edward J. Feil, Klaus Kurtenbach, Gabriele Margos. Environmental Microbiology. 13(1) 184-192. • Analysing the Genetic Diversity of Ixodes ricinus ticks using Multilocus Sequence Typing. Ruth E. Dinnis, Frederik Seelig, Antra Bormane, Michael Donaghy, Stephanie A. Vollmer, Edward J. Feil, Gabriele Margos, Klaus Kurtenbach. Submitted to Ticks and tick-borne diseases. See Appendix E for a current version of the manuscript. iv Abstract Abstract The hard tick Ixodes ricinus is one of the most important species of disease vectors worldwide. It transmits a variety of pathogens, including spirochaetes that are the causative agent of Lyme borreliosis (LB) in humans. This study aimed at analysing different aspects of the ecology, molecular evolution, and microbial associations of I. ricinus. A novel scheme for the phylogenetic analysis and genotyping of I. ricinus was established as part of this study. Phylogeographic clustering of I. ricinus samples from different European countries was observed, while samples from two different sites in Southwest England did not show spatial differentiation. The ecology and host abundance in these two habitats was assessed. Differences in the density of questing ticks and in the abundance of rodent hosts were observed. Both sites exhibited low densities of rodents and of ticks infesting them. A blood meal analysis revealed high proportions of mixed feedings and showed artiodactyls to be a main host group for immature I. ricinus ticks from Britain. The prevalence rates of Wolbachia endobacteria in British I. ricinus samples were higher than rates found in samples from other European countries. The unique endosymbiont Midichloria was detected in all female I. ricinus ticks that were screened. A newly developed multi gene analysis of Midichloria samples from six European countries showed a largely coordinated phylogeography with their tick hosts. Taken together, the findings of this thesis demonstrate that British I. ricinus ticks differ from their European counterparts in several ways, which has implications for the epidemiology of infectious diseases transmitted by this vector. v Table of contents Table of contents Cover sheet Acknowledgements iii Publications iv Abstract v Table of contents vi List of figures viii List of Tables x List of abbreviations xii 1. General introduction 15 1.1 A short history of ticks 15 1.2 General biology of Ixodes ticks 16 1.3 Pathogens transmitted by Ixodes ticks 26 1.4 Phylogenetics and multilocus sequence typing (MLST) of ticks 30 1.5 Overall aims and objectives of the sections in this thesis 33 2. Materials and methods 35 2.1 Field methods 35 2.2 Lab methods 42 2.3 Computer-based methods 50 3. Phylogenetic structure of Ixodes ticks in Europe and North America 53 3.1 Introduction 53 3.2 Results 57 3.3 Discussion 66 3.4 Conclusions 74 4. Environmental conditions in two tick habitats near Bath, UK 75 4.1 Introduction 75 4.2 Results 76 4.3 Discussion 93 4.4 Conclusions 101 5. Host blood meal analysis of I. ricinus samples 102 5.1 Introduction 102 5.2 Results 105 5.3 Discussion 125 5.4 Conclusions 131 6. Endobacterial fauna of I. ricinus 132 6.1 Introduction 132 vi Table of contents 6.2 Results 134 6.3 Discussion 144 6.4 Conclusions 149 7. General Discussion 150 7.1 Summary of findings 150 7.2 Discussion 151 7.3 Future work 154 7.4 Final summary 155 8. Bibliography 156 Appendices 177 A. List of tick collection sites 177 B. PCR conditions 178 C. List of BMA oligo probes 180 D. Scanned slides of BMA films 182 E. Manuscript of I. ricinus mtMLST paper by Dinnis et al. 195 vii List of figures List of figures Chapter 1: Fig. 1.1. General phylogeny of the Acari. Fig. 1.2. Phylogeny of the families and subfamilies of the suborder Ixodida. Fig. 1.3. Bayesian phylogenetic inference of 27 Ixodes species, based on 16S rDNA sequences. Fig. 1.4. General anatomic features of a female ixodid tick. Fig. 1.5. Life cycle of Ixodes ricinus. Fig. 1.6. Geographical distribution of four Ixodes species. Fig. 1.7. Genome organisation of non-Australasian Ixodes ticks Chapter 2: Fig. 2.1. Satellite image of the area surrounding the main campus of Bath University Fig. 2.2. Terrain contour map of the area surrounding the main campus of Bath University Fig. 2.3. Parts of a Longworth trap. Fig. 2.4. Sexual characteristics of male and female rodents. Fig. 2.5. Characteristic features of I. ricinus anatomy. Chapter 3: Fig. 3.1. Map of established and reported distribution of the Lyme disease vectors Ixodes scapularis and I. pacificus, by county, United States, 1907-1996. Fig. 3.2. Geographical distribution of reported human cases of Lyme disease in the continental United States in 2009. Fig. 3.3. Phylogenetic reconstruction inferred from the concatenated MLST mtDNA sequences of 40 ticks sampled in BW and RW in 2007 and 2008 using the Neighbour-Joining (NJ) method. Fig. 3.4. Phylogenetic reconstruction inferred from the concatenated MLST mtDNA sequences of 40 ticks sampled in BW and RW in 2007 and 2008 using the Maximum Likelihood (ML) method. Fig. 3.5. Phylogenetic reconstruction inferred from the concatenated MLST mtDNA sequences of 37 borrelia-positive and negative ticks sampled in BW and RW in 2006 using the Neighbour- Joining (NJ) method. Fig. 3.6. Phylogenetic reconstruction inferred from the concatenated MLST mtDNA sequences of 37 borrelia-positive and negative ticks sampled in BW and RW in 2006 using the Maximum Likelihood (ML) method. Fig. 3.7. Phylogenetic reconstruction inferred from the concatenated MLST mtDNA sequences of 40 ticks sampled in Latvia and Britain in 2007 using the Neighbour-Joining (NJ) method. Fig. 3.8.
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