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The Spatial Scale of Speciation and Patterns of Diversity Yael Kisel

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The spatial scale of speciation and patterns of diversity Yael Kisel A thesis submitted for the degree of Doctor of Philosophy of the University of London Division of Biology Imperial College London Silwood Park Campus December 2010 Abstract Many environmental factors and taxon traits have been studied as potential controllers of diversification, but there is no consensus as to which are most important or how to link them into a general theory of diversification. I hypothesise that diversification is strongly controlled by the interaction between area and clades’ spatial scales of speciation, or the minimum amount of area they require for speciation to occur. Furthermore, I hypothesise that the spatial scale of speciation is controlled by population genetic characteristics of clades, as speciation is ultimately a process of population divergence. In this thesis, I quantify taxonomic variation in the spatial scale of speciation, test whether it can be explained by variation in population genetics and evaluate whether it can explain taxonomic patterns of diversity. Using a survey of speciation events on isolated oceanic islands, I show that the spatial scale of speciation varies greatly between birds, lizards, snails, bats, carnivorous mammals, lepidoptera, angiosperms and ferns. I also use a meta-analysis of population genetic data collected from the literature to show that the minimum area for speciation of these groups correlates strongly with their average level of gene flow. I then test the link between population genetics and diversification by comparing population genetic characteristics of sister clades of tropical orchids that differ greatly in species richness. Contrary to expectation, levels of gene flow, genetic drift and local adaptation do not correlate directly with rates of diversification. However, there is some evidence for an interaction between species range size and gene flow in controlling diversification. This thesis supports a framework based on the interaction between area and the spatial scale of speciation as a useful foundation for general theories of diversification. It also highlights the potential for using a comparative population genetic approach in macroevolutionary studies. 2 Acknowledgements First, I would like to thank Tim Barraclough and Mark Chase for all their support and patience. I am also grateful to NSF, the Imperial College Deputy Rector's Scholarship, the University of London Central Research Fund, the Kew Bentham-Moxon Trust, and Sigma Xi for funding my work. In Costa Rica, I especially thank Diego Bogarín, who helped me with everything. I am very grateful to Jorge Warner for making me welcome at the Jardín Botánico Lankester and helping me with permits. Thanks also to many others at JBL: Franco Pupulin for advice; Rei and Rafa and Adam Karremans for coming on field trips; Allan and Enzo Salas for helping me settle in; and Socorro for dealing with paperwork. Thanks to the helpful staff of SINAC, especially Javier Guevara, Roger Blanco and Oscar Masis, and to UCR reserve director Ronald Sanchez. Thanks also to the owners of Bosque de Paz Reserve, and Melania Muñoz for organizing my visit there; to the owners of the Rara Avis Reserve; and to Freddy and Katia who allowed me to collect on their land. Great thanks to my fieldwork volunteers, Ryan Phillips, Julia Hu, Paul Renshaw and Kath Castillo. Finally, thanks to Fanny Bonilla and Carlos Piedra for hosting us so warmly. In the lab, my thanks first to Martyn Powell, who took on the task of teaching me AFLPs and answered my never-ending questions thereafter. I am also very grateful to Vincent Savolainen for allowing me to use his group’s lab facilities. Thanks to Robyn Cowan and Ovidiu Paun for in-depth talks about AFLP methodology and troubleshooting. Special thanks to Helen Hipperson for troubleshooting help, support and empathy. Thanks to Thomas Hahn for trying hard to figure out my AFLP troubles over email. Finally, thanks to everyone in the Savolainen lab for helping me find my feet with labwork, in particular Haris Saslis-Lagoudakis, Hanno Schaefer, Guillaume Besnard, Silvana del Vecchio, Paul Rymer and Alex Papadopulos. Thanks to Christian Lexer, Ally Phillimore and Alex Pigot for many illuminating discussions, and to all my friendly labmates, especially Diego Fontaneto. Thanks to Diana Anderson and Christine Short for cheerful help with everything administrative, and John Williams and the security crew for opening doors and solving problems. Thanks to the whole friendly Silwood community for making my PhD years so enjoyable, with special mention to Kat, Martina, Irka, Geraldine, Sally, Susanne, and Alice. Immense thanks to the house: Lynsey, Ellie and Lena for everything, but especially keeping me sane. Thanks to Bruce Tiffney, for inspiring me to be a passionate scientist and giving me the idea to go to the UK. Thanks to my parents for their unwavering support, even after I decided to move to a country 8 time zones away. And finally, thanks to Martin, for field help, lab help, R help, formatting help, numerous bloody marys and much more. 3 Declaration of originality I declare that all the work presented in this thesis is my own original research, with the following acknowledgements for each chapter: Chapter 2 has been published in slightly modified form in American Naturalist. It was written in collaboration with Tim Barraclough and made use of unpublished checklist data generously provided by Shai Meiri, Ana M. C. Santos, Roberto S. Gómez, Tod F. Stuessy and Christophe Thebaud. It was also greatly improved by suggestions from Jonathan Davies, Joaquin Hortal, Christian Lexer, Shai Meiri, Lynsey McInnes, Ally Phillimore, Andy Purvis, Vincent Savolainen and two anonymous reviewers. Chapters 3 and 4 made use of data-formatting and analysis scripts for R written by Martin Turjak. 4 Table of Contents Table of Contents Abstract ............................................................................................................................... 2 Acknowledgements ............................................................................................................ 3 Declaration of originality .................................................................................................. 4 Table of Contents ............................................................................................................... 5 List of Figures ..................................................................................................................... 8 List of Tables ...................................................................................................................... 9 List of Equations .............................................................................................................. 10 Chapter 1. Introduction.................................................................................................. 11 Comparative methods for studying variation in diversity .............................................. 11 What controls variation in diversity? Organism traits versus environmental variables . 13 A proposed framework for understanding variation in diversification .......................... 15 Approach and aims ......................................................................................................... 21 Summary of aims ........................................................................................................... 23 Chapter 2. Using oceanic islands to measure the spatial scale of speciation and its association with gene flow ............................................................................................... 24 Introduction .................................................................................................................... 24 Materials and Methods ................................................................................................... 30 Island selection and data collection ........................................................................... 30 Island species data collection ..................................................................................... 31 Identification of speciation events .............................................................................. 33 Adding phylogenetic information ............................................................................... 35 Statistical analysis of the speciation-area relationship .............................................. 36 Gene flow data ............................................................................................................ 37 Gene flow analyses ..................................................................................................... 40 Results ............................................................................................................................ 43 5 Table of Contents Data availability and quality ...................................................................................... 43 Quantifying the speciation-area relationship ............................................................. 43 Measuring minimum areas for speciation .................................................................. 47 Testing the importance of area when other environmental variables are included ... 48 The effect of gene flow ................................................................................................ 52 Discussion .....................................................................................................................
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