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Taxonomy Phylogeny and Eco Biogeography of Southern Taxonomy, phylogeny and eco-biogeography of southern African white-eyes (Zosterops spp.) Aves: Order Passeriformes Family: Zosteropidae By Graeme Oatley Thesis presented for the Degree of DOCTOR OF PHILOSOPHY Faculty of Science UNIVERSITY OF CAPE TOWN DST/NRF Centre of Excellence at theTown Percy FitzPatrick Institute of African Ornithology Department of Zoology UNIVERSITY OF CAPECape TOWN Privateof Bag X3 Rondebosch, 7701 South Africa Principal supervisor: Professor Timothy M. Crowe, DST/NRF Centre of Excellence at University of Cape Town, Percy FitzPatrick Institute of African Ornithology, Department of Zoology, Private Bag X3, University Rondebosch 7701 South Africa E-mail [email protected] Co-supervisor: Professor Rauri C.K. Bowie, Museum of Vertebrate Zoology & Museum of Vertebrate Zoology and Department of Integrative Biology, 3101 Valley Life Science Building, University of California, Berkeley, CA 94720- 3160, USA CA, USA E-mail [email protected] August 2011 Table of contents Page Taxonomy, phylogeny and biogeography of southern African white-eyes (Zosterops spp.) Aves: Order Passeriforms, Family: Zosteropidae Frontispiece vii Acknowledgments viii Abstract 1 Chapter 1 4 An overview of the taxonomy, phylogeny and eco-biogeography of southern African White-eyes (Zosterops spp.) 1.1. Introduction Town 1.1.1. White-eyes 1.1.2. Systematics 1.2. Taxonomic history Cape 1.2.1. Early days of 1.2.2. Moreau 1.2.3. Skead 1.2.4. Clancey 1.2.5.University Status quo 1.3. Summary 1.4. Hypotheses to be investigated Tables Figures i Chapter 2 27 The use of subspecies in the systematics of southern African white-eyes: historical entities or eco-geographic variants 2.1. Abstract 2.2. Introduction 2.3. Methods 2.3.1. Taxon sampling 2.3.2. Characters 2.3.3. Statistical analyses 2.3.4. Assumed taxa as ‘hypotheses’ 2.4. Results Town 2.4.1. Morphometric characters 2.4.2. Plumage colour scores Cape 2.4.3. Combined data of 2.4.4. Univariate and phylogenetic analyses 2.5. Discussion 2.5.1. Putative Zosterops taxa 2.5.2.University Four Zosterops taxa 2.6. Conclusion Tables Figures ii Chapter 3 63 The utility of song and contact call characters in the systematics of four African white- eye species (Zosterops spp.) 3.1. Abstract 3.2. Introduction 3.3. Methods 3.3.1. Vocal sampling 3.3.2. Vocal measurements 3.3.3. Analyses 3.4. Results 3.4.1. Song analyses Town 3.4.2. Call analyses 3.5. Discussion Cape Tables of Figures Chapter 4 81 A multi-locus phylogeny for southern African White-eye Zosterops taxa indicates interbreeding betweenUniversity non-sister taxa 4.1. Abstract 4.2. Introduction 4.3. Material and methods 4.3.1. Sampling 4.3.2. DNA extraction and PCR amplification 4.3.3. Phylogenetic analyses – Mitochondrial DNA 4.3.4. Phylogenetic inference – Nuclear DNA and combined analyses iii 4.3.5. Species tree inference 4.3.6. Morphospace and Environmental analyses 4.4. Results 4.4.1. Zosterops phylogeny – Mitochondrial DNA 4.4.2. Zosterops phylogeny – Nuclear DNA 4.4.3. Gene trees versus Species trees 4.4.4. Estimation of divergence times 4.4.5. Morphospace and Environmental analyses 4.5. Discussion 4.5.1. Molecular taxonomy of southern African Zosterops 4.5.2. Is there agreement with other lines of evidence?Town 4.5.3. Non-sister taxon hybridization 4.5.4. African white-eye diversificationCape Tables of Figures Chapter 5 116 Multi-locus phylogeography of southern African White-eyes (Zosterops spp.) reveals phenotypic divergenceUniversity across habitat boundaries with gene flow and introgressive hybridization after secondary contact 5.1. Abstract 5.2. Introduction 5.3. Methods 5.3.1. Sampling 5.3.2. DNA extraction and PCR amplification 5.3.3. Selection and recombination iv 5.3.4. Phasing of nuclear data 5.3.5. Population genetic analyses 5.3.6. Coalescent based estimates of gene flow and divergence times 5.3.7. Environmental space analysis 5.4. Results 5.4.1. Selection and recombination 5.4.2. Mitochondrial DNA 5.4.3. Nuclear DNA 5.4.3.1. CHD1 Town 5.4.3.2. MUSK 5.4.3.3. GAPDH Cape 5.4.3.4. TGFβ2 of 5.4.4. Population structure 5.4.5. Gene flow and population divergence 5.4.5.1. Z. capensis and Z. virens University 5.4.5.2. Z. virens and Z. pallidus 5.4.5.3. Z. capensis and Z. pallidus 5.4.5.4. Z. virens and Z. senegalensis 5.4.6. Environmental space 5.5. Discussion 5.5.1. Genetic structure and Biome affects v 5.5.2. Combined nuclear data, gene flow and hybridization 5.5.3. Taxon histories and inferences about southern African biogeography 5.5.3.1. Zosterops pallidus 5.5.3.2. Zosterops capensis and Zosterops virens 5.5.3.3. Zosterops senegalensis Tables Figures Chapter 6 173 Conclusions and future prospects 6.1. Morphology Town 6.2. Vocalizations 6.3. Molecular phylogeny Cape 6.4. Molecular phylogeography of 6.5. Hypotheses revisited 6.6. Final taxonomic conclusions 6.6.1. Southern African Zosterops taxonomy and systematics 6.7. Future prospectsUniversity References 193 vi Town Cape of University Frontispiece: Southern African Zosterops species and subspecies as recognized by, and taken from, Skead (1967). vii Acknowledgements My deepest thanks go to my two PhD supervisors, Prof. Timothy Crowe and Prof. Rauri Bowie. Your support, advice, feedback and motivation have been invaluable to the completion of this work. I have experienced and learned so much from you both, something that I will always be grateful for. I am very proud to have been associated with two highly successful scientists. The support outside of academics has contributed more than I could ever imagine to in helping me to finish this project. To my family: to my mom Dianne, my dad John and my sister Sam, thank-you. There was always someone to speak to and offer support during the tough times. Your encouragement and knowing that I could count on you has made the journey through the past five years so much easier to manage. Town To Shannon: Your support, encouragement and belief in me during the course of my work have been tremendous. I know I will never everCape be able to repay you for all that you did for me. Thank-you. of To Maria José: Thank-you for pushing me and showing me that anything is possible. Your impact on my way of thinking and approach to life has helped along the path in life I want to take from now on. Gracias. Fieldwork hasUniversity taken up a lot of my time during this PhD work, and this has afforded me the opportunity to work with and meet many new people. Most of you have become good friends, and your support in the field and outside of it has been fantastic. I know that our friendship will continue for years to come. So to all those of you that I have had the priviledge of spending time in the field with, thank-you: Ian “Been” Little, Jérôme Fuchs, Lisa Nupen (sorry about that time in the Karoo), Owen Davies, Ângela Ribeiro, Hanneline Smit, Sampath Lokugalappatti, Potiphar Kaliba (and your staff at the Museum of Malawi), Terence Suinyuy, Tom Gnoske, Gary Voelker, Verna Bowie and Penn Llyod. viii To all members the Botany Systematics Lab at UCT, the Molecular lab at the University of Stellenbosch and the Evolutionary Genetics Lab at the University of California in Berkeley, thank-you for teaching me my way around and for helping me when I often got stuck. Thank-you all for your invaluable help. A lot of the work done for this PhD could not be completed without the help of many people around South Africa. Thanks to those bird ringers that sent me many white-eye samples: Arnold vd Westhuizen, Kobie Raijmakers, Craig Symes, Dawie de Swardt, Joseph Heymans and Peter Nupen. A big thank-you to the numerous land owners that allowed us to collect samples on their property; also a special thanks to the members of the birding community that pointed me in the right direction for elusive samples: Neil Smith, Hugh Chittenden, Dave Weaver and his family, Zorb and Judy Caryer,Town Ben Smit, and Trevor and Jocelyn Smit. Finally, thank-you to the museums around South Africa for loaning the hundreds of white-eye specimens that I used in thisCape study: Rick Nuttal and Dawie de Swardt at the National Museum in Bloemfontein; Davidof Allen at the Durban Museum, staff at the East London and the Transvaal Museum. Finally, thank-you to the National Research Foundation of South Africa and the University of Cape Town for financial support. University ix Abstract White-eyes (Family Zosteropidae) are small passerine birds, with many species possessing a distinct ring of white feathers around the eye, while varying in underpart plumage colouration. There are currently 97 species within 13 genera placed in the Zosteropidae, occurring in Africa, Asia, Australia and Oceania. The most diverse genus, Zosterops, currently comprises 75 species which include all southern African white-eyes. At present, number of southern African Zosterops species recognized varies from one to three. Differing views have been adopted over the past 75 years, with taxa either being split according to underpart colouration or lumped together due to interbreeding between taxa. The aim of this study was to incorporate all lines of evidence to establish the true taxonomy and phylogeny of southern African Zosterops. CharacterTown data sets used include plumage and morphometric measures, vocal characters and molecular (mitochondrial and nuclear) DNA sequences. A broad scale phylogeographicCape analysis was also performed to establish the evolutionary process driving theof diversity observed among these birds.
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