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Biotic Interactions and Species Diversification in Southern African Biodiversity Hotspots

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Biotic Interactions and Species Diversification in Southern African Biodiversity Hotspots Biotic interactions and species diversification in southern African biodiversity hotspots Jan Schnitzler A thesis submitted for the degree of Doctor of Philosophy from the Division of Biology, Department of Life Sciences, Imperial College London September 2009 2 Abstract The south-western tip of Africa holds unique levels of species richness and endemism, and contains two hotspots of biodiversity: the Cape Floristic Region and the Succulent Karoo. Several hypotheses have been proposed to explain the radiation of the region’s diverse flora. However, due to the lack of comprehensive, comparative studies, the major forces that drive plant diversification have remained unclear. My thesis combines near-complete species- level molecular phylogenies with detailed biological, ecological and biogeographical information to investigate the evolutionary processes generating southern Africa's exceptional plant diversity. I demonstrate that in the genus Babiana (Iridaceae) climatic niches retain a high degree of phylogenetic conservatism, and show that species of Babiana were only able to successfully extend their range into new biomes with the establishment of more favourable climates. Additionally, results indicate that floral characters in Babiana evolve according to a new 'reversible shift' model, which better explains the evolution of pollination systems through multi-directional transitions in a diverse pollinator environment. These findings challenge the commonly held idea that floral specialisation is an evolutionary dead-end and offer new perspectives towards our understanding of plant-pollinator interactions. Analyses of a comprehensive data set of four large Cape clades show that the temporal dynamics of plant radiations in southern Africa confirm that the flora represents a combination of ancient and young radiations, and that diversification rates have remained constant through time. Finally, I reveal that although several biotic and abiotic factors contribute to the diversity, soil-type shifts is the most important driver of plant diversification in southern Africa. Together with complex geomorphological conditions, this factor, rather than pollinator 3 specialisation or phenological divergence, has given rise to the exceptional diversity found in this region today. Comparisons with other biodiversity hotspots, especially those with Mediterranean climates, will reveal whether this is a global scenario for the evolution of hyper-diverse floras. 4 Declaration I confirm that all work presented in this thesis is my own with the following acknowledgements: Parts of the data used in chapters 4 and 5 were contributed by colleagues. Martyn Powell provided new sequences for Moraea, Peter Goldblatt compiled data on the distribution and traits of Moraea, Steven Boatwright and Tony Rebelo provided parts of the distribution data for Podalyrieae and Protea, respectively. The use of any materials from other sources is fully acknowledged throughout this thesis. Jan Schnitzler London, September 2009 5 Acknowledgements First and foremost, I would like to thank my supervisors Vincent Savolainen and Timothy Barraclough for their advice, knowledge and inspiration over the past few years. I am very grateful to Peter Goldblatt and John Manning for their expertise and enthusiasm for this project. Furthermore, I thank Ingrid Nänni, Krytal Tolley and Koos Roux for the provision of material and help during collecting trips. I am indebted to many colleagues at the Royal Botanic Gardens, Kew for support, expertise in the lab and helpful discussions, in particular Mark Chase, Felix Forest, Laszlo Czsiba and Edith Kapinos. Thanks also to Dion, Rhian, Jimmy, Guillaume and Jon. A big thanks to the past and present members of the Savolainen lab: Haris, Silvana, Hanno, Andy, Rob, Guillaume, Helen, Matthieu and Richard. Think big! I am particularly grateful to Omar Fiz, Paul Rymer, and Alex Papadopulos for discussions and proofreading. Martyn Powell deserves special mentioning: thanks not only for your help in the lab, but also for introducing me to the peculiar game of cricket. Special thanks also to Yael Kisel and Lynsey McInnes. This work was funded by a Marie Curie fellowship of the European Commission, as part of the FP6 Early-Stage Training Network “HOTSPOTS – Understanding and Conserving Earth’s Biodiversity Hotspots” (MEST-CT-2005-020561) and I would like to thank my fellow HOTSPOTS students for an unforgettable time, whether discussing conservation strategies, ectoparasites, or life, the universe and everything. 6 Besonderer Dank gilt meiner Familie. Meiner Schwester Sonja für Unterstützung vor allem für ein spannendes Rennen um den ersten Abschluss der Disseratation. Meinen Eltern danke ich für Ihre beständige Hilfe und Unterstützung. Diese Arbeit ist Euch gewidmet. 7 "If we look to the large size and varied stations of New Zealand, extending over 780 miles of latitude, and compare its flowering plants, only 750 in number, with those on an equal area at the Cape of Good Hope or in Australia, we must, I think, admit that something quite independently of any difference in physical conditions has caused so great a difference in number." (Darwin, 1859) "La nature est une source inépuisable de recherches; et, à mesure que le domaine des sciences s'étend, elle présente, à ceux qui savent l'interroger, des faces sous lesquelles on ne l'avoit point encore examinée." (Alexander von Humboldt, 1815) 8 Table of Contents ABSTRACT................................................................................................................2 DECLARATION .........................................................................................................4 ACKNOWLEDGEMENTS............................................................................................5 TABLE OF CONTENTS ..............................................................................................8 LIST OF FIGURES ...................................................................................................12 LIST OF TABLES.....................................................................................................14 CHAPTER 1: INTRODUCTION.................................................................................15 1.1 Biodiversity Hotspots.................................................................................15 1.2 Plant diversity in southern Africa ............................................................17 1.3 Evolution of diversity in the Greater Cape Floristic Region (GFCR) ..20 1.4 Thesis aims and outline .............................................................................22 CHAPTER 2: PHYLOGEOGRAPHY OF THE GENUS BABIANA (CROCOIDEAE: IRIDACEAE) INFERRED FROM PLASTID AND NUCLEAR DNA SEQUENCES............24 Introduction......................................................................................................24 Materials and Methods....................................................................................26 PCR Amplification, Sequencing and Alignment...........................................26 Sequence data and analyses ...........................................................................27 Species distributions ......................................................................................30 Results...............................................................................................................32 Phylogenetic analyses....................................................................................32 Patterns of species diversity and range evolution..........................................38 Discussion .........................................................................................................45 9 Sequence variability and phylogenetic incongruence....................................45 Systematics of Babiana..................................................................................46 Biogeography.................................................................................................48 Conclusions.......................................................................................................51 CHAPTER 3: THE COMPLEXITY OF PLANT-POLLINATOR COEVOLUTION IN A BIODIVERSITY HOTSPOT ........................................................................................52 Introduction......................................................................................................52 Materials and Methods....................................................................................54 Taxon sampling and phylogenetic analysis ...................................................54 Principal Coordinate Analysis (PCoA)..........................................................54 Analysis of independent contrasts .................................................................55 Reconstruction of pollinator shifts and models of evolution.........................56 Results...............................................................................................................58 Morphological trait analysis ..........................................................................58 Tube length variation within and between pollination syndromes................58 Pollinator shifts..............................................................................................63 Discussion .........................................................................................................69 Conclusions.......................................................................................................74
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