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Avian Phylogeny and Divergence Times Based on Mitogenomic

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Avian Phylogeny and Divergence Times Based on Mitogenomic 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. Avian phylogeny and divergence times based on mitogenomic sequences Kerryn Elizabeth Slack 2012 A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Genetics Institute of Molecular BioSciences Massey University Palmerston North, New Zealand page i Abstract Despite decades of research using a variety of data sources (such as morphological, paleontological, immunological, DNA hybridization and short DNA sequences) both the relationships between modern bird orders and their times of origin remain uncertain. Complete mitochondrial (mt) genomes have been extensively used to study mammalian and fish evolution. However, at the very beginning of my study only the chicken mt sequence was available for birds, though seven more avian mt genomes were published soon after. In order to address these issues, I sequenced eight new bird mt genomes: four (penguin, albatross, petrel and loon) from previously unrepresented orders and four (goose, brush-turkey, gull and lyrebird) to provide improved taxon sampling. Adding these taxa to the avian mt genome dataset aids in resolving deep bird phylogeny and confirms the traditional placement of the root of the avian tree (between paleognaths and neognaths). In addition to the mt genomes, in a collaboration between paleontologists and molecular biologists, the oldest known penguin fossils (which date from 61- 62 million years ago) are described. These fossils are from the Waipara Greensand, North Canterbury, New Zealand, and establish an excellent calibration point for estimating avian divergence times. Bayesian analysis of the DNA sequence data, using the penguin calibration point plus two others, indicates a substantial radiation of modern bird orders in the Late Cretaceous (80 - 65 million years ago). Biotic interactions between modern birds and declining groups such as pterosaurs and early bird groups (e.g. Hesperornis and Ichthyornis) may thus have played an important role during this time. page ii Acknowledgements This thesis is for my family – Mum, Dad, Jude, Stu and Buzz: THANK YOU for your support, your encouragement and, above all, your patience! Words cannot express my gratitude to my supervisors: David Penny (Professor of Theoretical Biology and former Co-Director, Allan Wilson Center for Molecular Ecology and Evolution, Institute of Molecular BioSciences, Massey University, Palmerston North, New Zealand) – more than just a supervisor: a true friend, colleague and mentor; Mike Hendy (Professor of Mathematical Biology and founding Executive Director, Allan Wilson Center for Molecular Ecology and Evolution, Massey University) – I always appreciate your dry sense of humour Mike!; Ulfur Arnason (Professor of Evolutionary Molecular Systematics, Department of Cell and Organism Biology, University of Lund, Lund, Sweden) – I’ll never forget the ‘rock party’ Ulfur!; and Bengt-Olle Bengtsson (Professor of Genetics, Department of Cell and Organism Biology, University of Lund) – always patient, always kind. Thanks also to my unofficial supervisor: Pete Lockhart (Institute of Molecular BioSciences, Massey University, Palmerston North, NZ) – the archetypal ‘absent-minded professor’ -. A big thanks to my other co-authors: Axel Janke (Professor of Ecological Genomics, Goethe University, Senckenberg, Frankfurt, Germany), G. L. (Abby) Harrison (University of Oxford, Oxford, U.K.), P. A. (Trish) McLenachan (Institute of Molecular BioSciences, Massey University, NZ), Matt J. Phillips (University of Queensland, Brisbane, Australia), Alan Cooper (Professor, University of Adelaide, Adelaide, Australia), Craig M. Jones (Institute of Geological and Nuclear Sciences, Lower Hutt, NZ), Tatsuro Ando (Department of Geology, University of Otago, Dunedin, NZ), R. Ewan Fordyce (Professor, Department of Geology, University of Otago, Dunedin, NZ), and Frederic Delsuc (Laboratoire de Paléontologie, Phylogénie et Paléobiologie, Institut des Sciences de l’Evolution, Université Montpellier II, Montpellier, France). My deepest appreciation to the following: Anette Gullberg (University of Lund) and Trish McLenachan, Abby Harrison, Alicia Gore, Gillian Gibb and Charmaine Carlisle (all of/formerly of Massey University) for technical assistance; Matt (‘font of vertebrate information’) Phillips and Fred Delsuc for assistance with analysis; and Tim White and Warwick Allen (both of Massey University) for their assistance with computer programs, for running analyses on the Helix supercomputer and for help with other computer matters. I would also like to thank all those who helped out, by sharing information, advice and access, in the preparation of the manuscripts, Te Papa for the use of facilities, Massey Interloans for sterling service and the anonymous reviewers who commented on the early manuscript drafts. page iii A huge thanks to my NZ friends and colleagues, especially Trish McLenachan, Abby Harrison, Alicia Gore, Gillian Gibb, Charmaine Carlisle, Matt Phillips, Pete Lockhart and Tim White, plus Mike Charleston, Ant Poole, Mort Piripi, Simon Hills, Olga Kardailsky, Andrew Clarke and Richard Carter, for friendship, fun, support and fascinating conversations. Thank you also to my Swedish friends and colleagues, including Anette Gullberg (again), Xiufeng Xu, Tina Ledje, Anna Härlid, Ann-Sofie Rasmussen, Björn Ursing, Christian Elmerot, Martin Johansson and all of the others within the Lund Department of Cell and Organism Biology who helped me out with various things. I would also like to thank all those I met at assorted conferences and seminars for reminding me that there is more to life than bird mitochondrial genomes and that science is both interesting and stimulating! I would like to thank Alan Tennyson and Sandy Bartle of Te Papa (Museum of NZ) for supplying the penguin and albatross samples and Rod Hitchmough (Department of Conservation, Wellington) for his hatchet job cutting them up (much appreciated Rod), Anette Gullberg (University of Lund) for obtaining the goose sample, Dick Gill (NZ Department of Conservation, Waikanae office) for the petrel and the gull, Einar Arnason (University of Iceland) and Thorvaldur Björnsson (Museum of Natural History, Reykjavik, Iceland) for the loon, Darryl Jones (Australian School of Environmental Studies, Griffith University, Brisbane) and Ian Owens (University of Queensland) for the brush-turkey and Cathy Nock (Centre for Animal Conservation Genetics, Southern Cross University [Lismore campus], New South Wales) for the lyrebird. The work carried out in this study was supported at different times by a Swedish Institute Guest Scholarship, a Massey University Doctoral Scholarship, a University of Lund (Department of Genetics) Summer Stipendium, a Sven and Lilly Lawski Stipendium, a University of Lund (Department of Genetics) Doktorandtjänst, the Jörgen Lindströms Stipendiefond, the Swedish Science Council, the Nilsson-Ehle Foundation, the Allan Wilson Center for Molecular Ecology and Evolution (a NZ Centre for Research Excellence) and the NZ Marsden Fund. page iv Chapter 1. Introduction This introduction provides background to some of the key issues in avian phylogeny up to the time my first paper on bird evolution was published - Slack et al. (2003; Chapter 2). The date of this publication defines the scope of the introduction, thus references after 2003 are generally not included in this chapter, although there are exceptions, such as Clements (2005) which is used for nomenclature, and Penny and Phillips (2004) which a gives a range of hypotheses to be tested. In my summary (Chapter 5) I give an updating of the current understanding of avian evolution. Class Aves consists of all extant birds (Neornithes) together with some extinct groups such as enantiornithines (‘opposite birds’), hesperornithids (toothed waterbirds) and icthyornithids (toothed seabirds). Birds are usually considered as one of the five main groups of vertebrates, the others being fish, amphibians, reptiles and mammals (although ‘reptiles’ is not a strictly monophyletic group). Avians are descended from non-mammalian reptiles (almost certainly theropod dinosaurs; see Cracraft 1988 and references therein) and can easily be distinguished from other vertebrates through morphological characteristics such as feathers, wings and beaks (among others). There are almost 10,000 species of extant modern birds and they are globally distributed, being found from the Arctic to the Antarctic, on every continent and most if not all islands, and in a huge variety of environments. Assuming that Neornithes are a monophyletic group, for which there is substantial evidence (see, for example, Cracraft 2001 and references therein), three main questions about neornithine evolution remain: 1. When and where did neornithines originate? 2. How are the main lineages of modern birds interrelated? 3. What has been their temporal and spatial pattern of diversification? Although all aspects of avian phylogeny are important in their own right, this study focuses on aspects of questions 2 and 3: 1. The avian tree. This is split into two subprojects: a) finding the root of the avian tree, and b) resolving some deep avian relationships. 2. Dating avian divergences using well-supported early fossils (i.e. how many lineages of modern birds existed before the Cretaceous-Tertiary
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