The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgementTown of the source. The thesis is to be used for private study or non- commercial research purposes only. Cape Published by the University ofof Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University Ecological and evolutionary processes in two southern African endemic birds Ângela M. Ribeiro Town Cape Dissertation presentedof for the Degree of Doctor of Philosophy in the Department of Zoology University of Cape Town University Cape Town, August 2011 DECLARATION I, Ângela Maria Oliveira Ribeiro, hereby declare that: i) the work presented in this thesis is my own and, ii) neither the substance nor any part of this thesis has been submitted or is to be submitted for a degree at this or other University. Town Cape of Cape Town, August 2011. University Town I chased lions, I climbed mountains, I dove deep. I rambled the jungle, I lived in a tank, I flu with strings,Cape I had private clouds and self-sunrises. I was a silent cold blue wind and a blooming springof flower. In my world, in my scene, within me, I recreated myself. Now, in the mighty silence of my dreams, in my scene, within me, I see your smile. UniversityI can swim, I can dance; we can fly with no fears, with no strings, until the end. And I still love. To the memory of Manuel Paço e Brito CONTENTS Preface i Acknowledgements ii Abstract iii Chapter Summary iv Chapter One 1 Introduction Two 11 Microsatellites in the Karoo Scrub-Robin, Cercotrichas coryphaeusTown: isolation and characterization of 13 autosomal and two sex-linked loci. Three 16 Microgeographic socio-genetic structure of an AfricanCape cooperative breeding passerine revealed: integrating behavioural and genetic data Four of 33 A tight balance between natural selection and gene flow in a southern African arid-zone endemic bird Five 57 Dynamics of a range expansion: placing adaptation in the context of the colonization of a new habitat Six University 80 Eco-geographical context of morphological and genetic divergence in a forest-dwelling Scrub- Robin of southeast Africa Seven 99 Conclusion References v Postface vi PREFACE Sleepwalk typewriter Oftentimes I find my memories sleepwalking to the imagination, where all the ephemerally disoriented memories unhappen in the same scene: a naked Baobab at the peaceful rhythm of the Indian Ocean waves; the mossy scent of the forest after a heavy rain with an eagerly roaring waterfall; the dazzling warm rays of a sunrise closely watched by beautiful Orion; the Townhollow sound of electric fences in the same tone of the cheerful carillon; a colourfully dressed woman carrying a tin of water, empress of the cool summer fog; the tart-sweet ripped guavas nurtured by the salty ocean smell; the shadow of blooming oaks over the wavy fiery red dunes; the beloved persons I lost for never in the same smile with the friends I gained for ever. All unhappening until the blue, red andCape green decide to sum up in the sky, and then shatter into the earth painting the most gorgeous and peaceful sunset one can witness. Memories; they all temporarily return to ‘happened’. I find myself whenof I imagine this beautiful journey. Imagine. University i ACKNOWLEDGEMENTS Completing my degree would not have been possible without the generosity of many people. It is a great pleasure to thank everyone, who have inspired, assisted and guided me in multiple ways. Foremost, I want to thank Rauri Bowie, my advisor. Rauri, thank you so much for giving me the opportunity to be a member of your lab, at UC Berkeley. I appreciated the freedom you gave me to find my way. I am grateful for your affability, patience, support and guidance throughout this journey. My most sincere and endless thank you! Penn Lloyd, my academic supervisor during the first two years of the programme, your help in the field was precious. I will never forget your hospitality when I first arrived in South Africa – thank you! Phil Hockey, I am grateful for your willingness to act as myTown academic supervisor and your thoughtful comments when revising my chapters – thanks so much! Ricardo Lopes, thanks for your support during the process of writing and submitting the FCT grant application and for joining me in the field. Cape I acknowledge the Fundação para a Ciênciaof e Tecnologia (FCT, Portugal) and the Department of Science and Technology and National Research Foundation (NRF, South Africa) for providing funding to conduct my research. I am grateful to the Animal Ethics Committee at the University of Cape Town for approving my research program. And for granting the research and collecting permits I thank: SAFRING, the South African National Parks; Northern Cape Department of Nature and Environmental Conservation; Free State Department of Tourism, Environment and Economic Affairs; Eastern Cape Department of Agriculture, EnvironmentUniversity and Tourism; and, the Department of Environment and Tourism Department of Namibia. Hugh Chittenden, Mark Brown, Dawie de Swardt, Joseline and Trevor Smit, Adrian Craig, Niel MacGregor, Rod and Cathy Molteno, Larry King, Ronnelle and Stoffel Visagie, Sharon Louw, David Pretorius and, Pieter Strauss: thank you for being fantastic hosts, helping with logistics in the field and for sharing your knowledge about the region, wildlife and particularly Scrub-Robins. I thank David Willard, Gary Voelker and Tom Gnoske (Field Museum, Chicago, USA), Dawie de Swardt (National Museum at Bloemfontein, Free State, South Africa), Joseph Heymans, Kobie Raijmakers, Craig Symes, and Peter Nupen, for providing biological samples. ii Andrew, the mesmerizing; Jay, the adorable; Roberta, the heartfelt; José, the amusing; Ricardo, the epicurean; Aninha, the generous; Jérôme, the ‘mais oui’ jocular: to all of you my utmost, deep and sincere gratitude. Thanks for your endless help and support, for the company, for your thoughtful insights, for discussing and reading so carefully my manuscripts, for the heavy doses of optimism and mostly, for the memorable and marvellous moments together. I very much appreciated your friendship, kindness and generosity throughout this intense journey. I love you all very much dear friends! Jérôme, Hanneline and Graeme, my field-office-labmates, I had a terrific time with you in the field! It was “baie, baie lekker!” Thanks very much for running for Scrub-Robins. Sandra, Marta, Buckley, Knud, Jon, Fujita, Mitzy, Kristal, Tânia, Michael, Luca, Potiphar, Sampath, Callan, Michael, Rowena: thanks for the wonderful times together! I was officially a Ph.D student at the University of Cape Town inTown South Africa. However, I spent most of my time at the Museum of Vertebrate Zoology, University of California at Berkeley. Berkeley had/has an intriguing simultaneous duality, which makes it unique and unforgettable: innovative and traditional, friendly and aloof, inspiring and disheartening, fulfilling and overwhelming, challenging and monotonous. Being a student in Berkeley was such a rewardingCape experience: scientifically and personally! I acknowledge Craig Moritz, the director of the ofMuseum, for allowing me to be part of the MVZ community. I extend my gratitude to everyone in the MVZ for welcoming and hosting me during these last four years – thanks very much! All the Bowie’s lab members are thanked for tirelessly listen to, discussing and reading my ideias. Cristina e Sara, obrigada por fazerem da distância geografica que nos separou um mero até logo. Encheu-me o coração cada uma das mensagens/presentes que me enviaram. Obrigada pela partilha! Avó Maria e Ermelinda,University embora a barreira tecnlogica tenha exacerbado a distância física, cada conversa foi fonte de alegria e felicidade. A vossa valentia foi e será sempre inspiradora e motivo de orgulho. Obrigada! Mãe e pai, obrigada pela constante presença, pelo apoio infinito. Sem a vossa generosidade e amor nada seria possível. Adoro-vos! Obrigada, Thank you, Dankie, Gracias, Merci! August, 2011 ii ABSTRACT Understanding the continuous process of divergence that leads to the formation of species requires the simultaneous think about ecology, evolution and its intertwining relationship. In this dissertation, I propose a population-level framework that integrates ecology and population genetics to rethink the mechanisms that promote divergence. To accomplish that I studied two southern African endemic Cercotrichas scrub-robins: C. coryphaeus and C. signata. Despite its phylogenetic proximity the two study species occupy the two ends of the habitat spectrum available in southern Africa: semi-arid Karoo vs. Forest. First, I combined behavioural ecology with individual-basedTown genetic data in the Karoo scrub- robin examined the role of social relationships in shaping mating patterns and dispersal behaviour and ultimately influence the evolution of dispersal. Second, using the knowledge obtained about the dispersal biology of the Karoo scrub-robin, I tested whether naturalCape selection can counter-balance gene flow and hence promote local adaptation along the aridity gradient that characterizes the range of the species. The results suggested that selective pressures on physiology,of mediated by the mtDNA genome, might facilitate the adaptation to new climatic conditions. Third, prompted by the previous findings, I examined the historical context of a spatial and demographic expansion to understand the role of natural selection in the colonization of a new environment, in the Karoo scrub-robin. Lastly, I evaluated how the eco- geographical context affects the divergence process in the forest-dweller C. signata. University iii CHAPTER SUMMARY The intellectual motivation for this dissertation was shed light on the mechanisms that promote population divergence and can ultimately lead to the formation of species, in an area of the world that is still understudied: the southern African subcontinent. My thesis consists of seven chapters. Chapter one is an introduction to the topics I proposed to address, and chapter seven the general conclusions from the research I developed and described in five interrelated chapters.