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The Role of Pathogens in Shaping Genetic Variation Within and Among Populations in an Island Bird

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The Role of Pathogens in Shaping Genetic Variation Within and Among Populations in an Island Bird The role of pathogens in shaping genetic variation within and among populations in an island bird Photo by Philip Lamb Claire Armstrong A thesis submitted for the degree of Doctor of Philosophy University of East Anglia School of Biological Sciences September 2018 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived therefrom must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. 0 Abstract This thesis aimed to investigate the role of pathogen-mediated selection in shaping patterns of genetic variation in Berthelot’s pipit Anthus berthelotii, a passerine endemic to the Macaronesian archipelagos of the Canary Islands, Madeira, and Selvagens. I used restriction-site associated DNA sequencing (RAD-seq) to investigate patterns of neutral diversity among Berthelot’s pipit populations, and in its sister species, the tawny pipit Anthus campestris, finding a loss of genome-wide diversity associated with colonisation history and genetic bottlenecks. I performed genome-wide association studies (GWAS) to identify genomic regions associated with malaria infection and bill length. I detected signatures of divergent selection around potential candidate genes related to immunity and metabolism, suggesting that these traits play roles in divergence and adaptation in this species. I then characterised genetic variation in Berthelot’s and tawny pipits at avian β-defensins (AvBDs), a key gene family of the innate immune system. Allelic richness decreased with increasing numbers of bottlenecks. However, some AvBDs showed elevated nucleotide diversity compared with genome-wide trends. We found no evidence of local adaptation or balancing selection in Berthelot’s pipits, suggesting that AvBD variation in this species is predominantly driven by genetic drift. Finally, I investigated whether malaria was driving fine-scale patterns of variation at SNPs identified in the earlier GWAS, and at the toll-like receptor 4 (TLR4) locus, a pathogen recognition receptor of the innate immune system, in two island populations. Both islands showed potential associations between malaria infection and TLR4 variation. In contrast, there was no association between a GWAS SNP and malaria risk in Tenerife, whereas in Porto Santo, the opposite trend to the original GWAS was found, potentially indicating local adaptation and population divergence. Overall, the evidence suggests that although functional variation in Berthelot’s pipits is strongly influenced by demographic history, adaptation to pathogens may be occurring within and between populations. 1 Acknowledgements I would first like to thank my supervisors David Richardson, Richard Davies and Lewis Spurgin. This work would not have been possible without their teaching and support over the past four years. Thank you for helping me through the hard times, for celebrating my achievements, and for encouraging me to have confidence in my abilities. I would like to thank Gavin Horsburgh, Helen Hipperson, Clemens Küpper and Terry Burke from the NERC Biomolecular Analysis Facility at the University of Sheffield, and Matt Clark and Lawrence Percival-Alwyn at the Earlham Institute, for all of their training, help and contributions to my first publication. I am grateful for the support of Deborah Dawson, Rachel Tucker and Andy Krupa, who facilitated my time in Sheffield. My fieldwork was made possible by a Heredity fieldwork grant from the Genetics Society, and by the Madeiran Natural Parks department, who generously offered us accommodation on Porto Santo. Thank you to Juan Carlos Illera for providing fieldwork training during our time on Madeira. I am very appreciative of the lab work carried out by Dom Hill, Molly Dunne and Maria- Elena Mannarelli, which greatly helped with analysing my fieldwork samples. Thank you to everyone at UEA who has made the last four years highly enjoyable. Special thanks to Natasha Senior, David Litchfield, Kris Sales and Jessie Gardner for being great friends and housemates. A massive thank you to Stephanie Hirsch, Sean McGregor and Bethan Edmunds for always being there through ups and downs. I would like to thank Virginia, Simon and Louise Lamb for being so welcoming, it’s been lovely getting to know you all. Thank you Mum and Dad for everything you’ve done for me over the years, and for always believing in me. You’ve helped so much to get me to where I am today, and I will always be grateful for that. Thank you Nick for being my big brother, Bekki for becoming part of the Armstrong family, and both of you for making me an auntie to Zak. Finally, I would like to thank Philip Lamb for your love and support over the past four years. I am so grateful for your patience and encouragement, and for always being there when things have been tough. Thank you for always trying to make me laugh, for your excellent pipit herding skills, and for being an all-round wonderful person. 2 Author contributions One of the chapters in this thesis has been published, and two manuscripts are currently in preparation. All chapters have involved collaboration. I am the lead author on all manuscripts, and have made the largest contribution to all. Chapter 2 consists of two original chapters that were combined into one large paper. Chapter 2. Armstrong C, Richardson DS, Hipperson H, Horsburgh GJ, Küpper C, Percival-Alwyn L, Clark M, Burke T, Spurgin LG (2018) Evolution Letters 2: 22-36 CA performed most of the lab work and bioinformatics, analysed the data and drafted the manuscript. Chapter 3. Armstrong C, González-Quevedo C, Spurgin LG, Richardson DS (In prep.) CA performed most of the lab work, analysed the data and drafted the manuscript. Chapter 4. Armstrong C, Davies RG, González-Quevedo C, Dunne M, Spurgin LG, Richardson DS (In prep.) CA collected the samples, performed part of the lab work, analysed the data and drafted the manuscript. 3 Contents Abstract ........................................................................................................................................ 1 Acknowledgements ...................................................................................................................... 2 Author contributions .................................................................................................................... 3 List of tables and figures ............................................................................................................... 6 Chapter 1. General introduction ................................................................................................... 9 1.1. Evolutionary drivers of genetic variation ..................................................................... 10 1.2. Defining neutral variation and demography ................................................................ 11 1.3. The genomic basis of adaptation ................................................................................. 13 1.4. Pathogen-mediated balancing selection ...................................................................... 14 1.5. Toll-like receptors ........................................................................................................ 17 1.6. Antimicrobial peptides and β-defensins ...................................................................... 20 1.7. Pathogen-mediated selection and adaptive variation in Berthelot’s pipit .................. 21 1.8. Thesis aims ................................................................................................................... 23 1.9. References ................................................................................................................... 23 Chapter 2. Genomic associations with bill length and disease reveal drift and selection across island bird populations ............................................................................................................... 38 2.1. Abstract ........................................................................................................................ 39 2.2. Introduction ................................................................................................................. 39 2.3. Methods ....................................................................................................................... 42 2.4. Results .......................................................................................................................... 50 2.5. Discussion .................................................................................................................... 63 2.6. References ................................................................................................................... 67 4 2.7. Supplementary Material .............................................................................................. 75 Chapter 3. Genetic drift outweighs selection to shape AvBD diversity in a bottlenecked island bird .............................................................................................................................................. 80 3.1. Abstract ........................................................................................................................ 81 3.2. Introduction ................................................................................................................. 81 3.3. Methods ......................................................................................................................
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