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Population Genetics, Biogeography and Ecological Interactions of the New Zealand Bellbird (Anthornis Melanura) and Their Avian Malaria Parasites

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Population Genetics, Biogeography and Ecological Interactions of the New Zealand Bellbird (Anthornis Melanura) and Their Avian Malaria Parasites Copyright is owned by the Author of the thesis. Permission is given for a copy to be downloaded by an individual for the purpose of research and private study only. The thesis may not be reproduced elsewhere without the permission of the Author. Population Genetics, Biogeography and Ecological Interactions of the New Zealand Bellbird (Anthornis melanura) and their Avian Malaria Parasites A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Zoology at Massey University, Albany, New Zealand Shauna Maureen Baillie September 2011 Abstract Adult female New Zealand bellbird (Photo: Jordi Segers) Singing adult male New Zealand bellbird (Photo: Rob Cross) Giemsa-stained blood smears from a bellbird at Tawharanui Regional Park infected with intracellular Plasmodium sp. Three adult male bellbirds at a sugar water feeder (arrows in upper and lower photos) on Tiritiri Matangi (Photo: Jordi Segers) (Photos: Gribbles Veterinary) Abct Abstract Habitat loss and redistribution of species has lead to population declines and loss of genetic diversity with serious implications to species survival on ecological and evolutionary scales. While there is no doubt that rapidly dwindling endangered populations require our immediate attention, studies on common species are equally important. The purpose of this thesis is to investigate the genetic connectivity, biogeographical relationships and host-parasite interactions of a common and widely distributed bird species, mainly because we want common species to remain common. Furthermore, I illustrate how studies such as this provide invaluable comparisons for sympatric endangered species. In this thesis, patterns of genetic variation of the New Zealand bellbird (Anthornis melanura) are delineated to assess their re-colonization potential among fragmented landscapes. Using a phylogeographic perspective I show how dispersal ability and secondary contact among isolated population fragments shape the evolutionary trajectory of a species. I also determine the biogeographical relationships between the bellbird host and its malaria parasites with key emphasis on host-parasite specificity. Finally, immunological trade-offs are investigated in disease epidemiology by examining host factors that influence malaria prevalence. I show that an immense capacity for dispersal has prevented divergence and shaped the high levels of genetic diversity and connectivity in bellbirds today. However, substantial genetic differentiation among subpopulations reflects recent habitat fragmentation. Based on these findings I conclude that continued habitat loss can lead to further reductions in gene flow, despite dispersal. Though restricted to northern populations, I provide evidence that the most abundant avian malaria lineage infecting bellbirds is likely an endemic Plasmodium (Novyella). This parasite exhibits bimodal seasonality and male-biased infections, but these relationships vary among subpopulations. Malaria prevalence appears to be governed by food availability and territory stability, thus habitat disturbance has repercussions to immune phenotype. With this thesis I advocate a re-thinking of conservation strategies toward spatial planning that enables ‘natural’ secondary contact among habitat fragments. Translocation is not necessary for all species. In addition to being the first study on seasonal and host factors affecting malaria patterns in the Southern Hemisphere, this thesis makes major contributions to science by elucidating some ecological relationships that underpin the evolution of immunity. i Acknowledgments First and foremost, I would like to dedicate this thesis to my mother, Diane Sylvester, in memoriam. Her intelligence and free-spirit are the true inspiration behind the undertaking of this thesis. I could not have done this thesis without the never failing support of my main supervisor Dr. Dianne Brunton (Director of the Ecology and Conservation Group, Institute of Natural Sciences, Albany Campus, Massey University, New Zealand). Dianne is an extraordinary person able to field various students, and somehow keep us happy while demanding the best from us. These traits are a rare combination in an individual, let alone a PhD supervisor (as a quick perusal of PhD Comics.com will illustrate) and I feel very lucky and privileged to have worked under her. The first ‘field ecology’ phase of my PhD thesis was spent at Massey University where in addition to conversations with Dr. Dianne Brunton. I am grateful to Dr. Rosemary Barraclough, Dr. Weihong Ji and Dr. Kevin Parker for helpful and incredibly knowledgeable discussions in the earlier phase of my thesis. For the second ‘genetics laboratory’ phase, Dr. Pete Ritchie welcomed me into his genetics lab at the School of Biological Sciences (SBS), Victoria University of Wellington, Kelburn Campus, Wellington, New Zealand. Dr. Ritchie was well equipped with the generosity, grace and patience required to accept a completely green-to-population- genetics PhD student into his lab. I am forever indebted that he took me in. Pete was an integral part of this thesis, I was very inspired by the work done and expertise within Pete’s lab group and learned so much from our weekly Population Genetics Lab Group Meetings. Gracious thanks especially to Jordi Segers, Morag Fordham and Simon Fordham who were my most dedicated field technicians. Many long days were spent wandering around in the forest on the North Island as well as offshore islands setting up and taking down mistnets. These three wonderful people extracted hundreds of birds of several difference species from the nets while I took blood and measured them at the banding table. They were always up for the long haul with not one complaint. I also want to thank my lovely friends Birgit Ziesemann and Barbara Egli who helped catch bellbirds at Hauturu during my last trip, and also to Miriam ii Ludbrook and Eva Krause who helped capture bellbirds at Tawharanui. At the Poor Knights Islands Michael Anderson and Yuri Shanas were crucial to fieldwork and in making that trip an incredible adventure. Additionally, I want to give special thanks to Ngati Wai Iwi Trust Board and particularly to Clive Stone for meeting with me and giving us the permission to visit and conduct my research within their wāhi tapu. Dr. Graeme Elliott of the New Zealand Department of Conservation (DoC) generously collected blood samples from the Auckland Islands. All blood collection from birds was performed under DoC permit, Auckland Regional Council (ARC) and Massey University Animal Ethics Committee (MUAEC). I extend many gracious thanks especially to my officemates at VUW including Sebastien Rioux-Paquette, Monica Gruber and Elizabeth Heeg for their energetic and inspired conversation and for sharing of their easy guru-like knowledge with regard to population genetics. Access to post-doctorate researchers such as Sebastien Rioux-Paquette, Hilary Miller, Kristina Ramstad and Christian Bödeker was important. Importantly, I also want to extend warm gratitude to the proverbial ‘cogs’ of SBS who include Mary Murray, Sandra Taylor, Patricia Stein, Paul Marsden and Delwyn Carter-Jarratt who were supportive and fun, and the latter two were stalwart soccer mates for the short while I overlapped with them on the field. My father, Dr. Robert Baillie, his wife Michelle and my two brothers Mark and Michael were always there for me in their respective quiet ways on the far side of the globe. I love the four of them very much. A special thanks to all the musos, especially Dr. Weihong Ji, for the celtic jam sessions that were so enjoyable over the past few years. Also, thanks to friends who were there to provide much needed diversions such as my rock climbing buddies who also doubled as Friday Happy Hour buddies from time to time. This study was funded by a Canadian Natural Science and Engineering Research Council (NSERC) PGS scholarship to SMB and the New Zealand Institute of Natural Sciences (INS) Massey University. Dr. Pete Ritchie covered a generous amount of consumables and primer costs while I worked in his genetics lab. Invaluable contributions from the New Zealand Ecological Society Hutton Fund, Tiritiri Supporters and Little Barrier Trust Fund were greatly appreciated over the course of this thesis. iii Thesis Structure and Format I have written this thesis as a collection of five scientific papers for publication in peer reviewed journals. An introductory chapter (Chapter One) precedes the five data chapters and is written for a general science audience that provides some background on the theory and analytical components of my thesis. This format has meant that some of the Introduction is repeated in the various Introductions throughout the thesis, but this is necessary for the reader to have a complete overview of the thesis. Chapter Seven is a synthesis that summarizes my findings and outlines my contributions to science and future research. Chapters Two to Six are data chapters that each stand as independent scientific papers. Within the text of these five data chapters, I used the plural first person because my supervisors are on these papers as co-authors. However, the study design, fieldwork, laboratory work and all statistical analyses and writing were performed by me with only supervisorial input from co-authors. During the process of my first population genetics chapter, Chapter Two, I presented my work at several stages to Dr. Pete Ritchie’s Population Genetics Discussion Group at Victoria University
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