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The Ecology and Evolution of Aspergillus Spp. Fungal Parasites in Honey Bees

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The Ecology and Evolution of Aspergillus Spp. Fungal Parasites in Honey Bees The Ecology and Evolution of Aspergillus spp. Fungal Parasites in Honey Bees Kirsten Foley Submitted in accordance with the requirements for the degree of Ph.D. The University of Leeds School of Biology May 2013 The candidate confirms that the work submitted is his/her own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated after each chapter. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Chapter 2 Foley, K., Fazio, G., Jensen, A. B., Hughes, W. O. H., 2012. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. J. Invertebr. Pathol. 111, 68–73. The candidate, Kirsten Foley, designed the experiments, carried out the experimental work, analysed the data and wrote the manuscript. GF assisted with the experimental work, specifically the collection of bee larvae. ABJ assisted with the design of the experiments and provided training. WOHH supervised the work, assisted with the design of the experiments, the data analysis and drafting of the manuscript. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. ⓒ 2013 The University of Leeds and Kirsten Foley 1 Acknowledgements There are many people I would like to thank for their help and support throughout the course of writing this thesis as well as those who helped me along the way. I would like to thank Dr. Emer Rogan, Dr. Sarah Culloty and Dr. Tom Kelly for their support, advice and for inspiring my enthusiasm for parasitology during my undergraduate years. A very special thank you to my supervisor Bill Hughes for all his help and advice, for having given me this opportunity and whose door was never closed throughout my three and a half years spent in the Hughes lab. A huge thank you to Bill Cadmore for all his help, wonderful company and for sharing his invaluable beekeeping expertise during the busy field season months. A warm thank you to all the lab members past and present, with whom I shared this time with including Geraldine Fazio, Judith Slaa, Rowena Mitchell, Pete Graystock, Kat Roberts, Sophie Evison and Adam Smith you are all wonderful people to work with. All the very best wishes to Paula Rosewarne who was the best flatmate anybody could have. To my cousins Ann, Eileen, Lizzie, Siobhan, Miriam, Karen and friends Mairead Behan, Michelle O’Sullivan, Helen Howard, Dave Penny and Sharon Baird for their generosity, visits, hospitality and many laughs during my time spent in Leeds. And finally, I would not have been able to return to study and achieve anything if it were not for the continuous support and encouragement from my parents, to them I am eternally grateful. 2 Abstract Evolution of virulence in parasites has profound effects on both host-parasite co- evolution and ecology and is influenced by environmental factors and the genotypes involved. Many parasite infections consist of multiple strains or species that are predicted to result in the evolution of more virulent strains that exploit the host less prudently. In opportunistic parasites, the dynamics and evolution of virulence are poorly understood as traditional epidemiological models do not adequately describe parasites capable of persisting outside of the host. In addition, as microbial pathogenicity may shift from opportunistic to obligatory strategies with time, knowledge of the evolutionary dynamics of opportunistic pathogens is crucial for predicting and understanding disease emergence. Aspergillus species of fungi have a ubiquitous distribution and are the etiological agents of stonebrood disease in honey bees. It is generally considered that stonebrood occurs rarely in honey bees, but the epidemiology and predisposing conditions for the disease are almost entirely unknown. In this study, I examine the occurrence, pathogenicity and competitive ability of Aspergillus spp. when infecting honey bees, as well as the effect of nutrition on host susceptibility and the adaptation of the fungi over the course of experimental evolution. A high prevalence and diversity of Aspergillus spp. isolates were identified following the screening of an apiary, and the pathogenicity of three species (A. flavus, A. nomius and A. phoenicis) was established. Further, in laboratory-reared larvae a nutritionally limited diet increased susceptibility to A. fumigatus. In a series of single- generation interspecific competition experiments between Aspergillus spp. and the obligate pathogen chalkbrood (Ascophaera apis), the virulence and fitness of dual infections were influenced by complex within-host interactions depending on the species involved, which ranged from synergistic to inhibitory effects. Finally, following serial passage of A. flavus and A. phoenicis in the honey bee larval hosts to determine the evolution of virulence and fitness, no evidence of host adaptation was observed, revealing the unpredictability of these asexually reproducing opportunistic pathogens. These findings illustrate a complex relationship between Aspergillus spp. and honey bees and emphasises the significant influence these ubiquitous organisms can have on the ecology and evolution of honey bees. 3 Table of Contents Acknowledgements.........................................................................................................2 Abstract...............................................................................................................................3 Table of Contents..............................................................................................................4 List of Tables......................................................................................................................7 List of Figures....................................................................................................................8 Chapter 1: General Introduction...............................................................................11 1.1 General Introduction...............................................................................................................11 1.2 The evolution of virulence and multiple infections...................................................12 1.3 Current concerns in honey bee health…………..............................................................13 1.4 Characteristics of social insect colonies: potential for disease.............................14 1.5 Honey bee immune defense.................................................................................................14 1.6 Genetic diversity and disease resistance........................................................................15 1.7 The genus Aspergillus..............................................................................................................16 1.8 Stonebrood...................................................................................................................................19 1.9 Chalkbrood...................................................................................................................................20 1.10 Studying the stonebrood and chalkbrood system...................................................22 1.11 Thesis aims................................................................................................................................24 Chapter 2: Prevalence of Aspergillus opportunistic fungal parasites in an apiary and their pathogenicity to honey bees.....................................................................26 2.1 Abstract..........................................................................................................................................26 2.2 Introduction.................................................................................................................................27 2.3 Materials and Methods............................................................................................................29 2.3.1 Aspergillus prevalence..........................................................................................29 2.3.2 Fungal identification and quantification.......................................................30 2.3.3 Aspergillus virulence in honey bee larvae......................................................31 2.3.4 Aspergillus flavus virulence in adult honey bees…………………................32 2.3.5 Statistical analysis...................................................................................................33 2.4 Results..............................................................................................................................................33 2.4.1 Colony level prevalence.........................................................................................33 2.4.2 Within-colony prevalence.....................................................................................34 2.4.3 Aspergillus diversity................................................................................................35 4 2.4.4 Dose response tests..................................................................................................39 2.5 Discussion......................................................................................................................................42 2.6 Acknowledgements....................................................................................................................45
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