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Phylogenetic and phenotypic divergence of an insular radiation of birds Richard Anthony Black Imperial College London, Department of Life Sciences Thesis submitted for the degree of Doctor of Philosophy 2010 1 General Abstract Evolutionary divergence of lineages is one of the key mechanisms underpinning large scale patterns in biogeography and biodiversity. Island systems have been highly influential in shaping theories of evolutionary diversification and here I use the insular Zosteropidae of the south west Pacific to investigate the roles of ecology and biogeography in promoting evolutionary divergence. Initially I build a phylogenetic tree of the study group and use it to reveal the pattern of colonisation and diversification. My results suggest a complex history of dispersal with the observed pattern most likely a result of repeated bouts of colonisation and extinction. I then use the new phylogeny to quantify the diversification rates of the Zosteropidae. I find a very high rate of lineage divergence and suggest the most likely explanation relates to extensive niche availability in the south west Pacific. I also find evidence for an overall slowdown in diversification combined with repeated bursts of accelerated speciation, consistent with a model of taxon cycles. I do not find evidence for sympatric speciation, however. Finally I combine morphological and phylogenetic data to investigate the mode of evolution, evidence for character displacement and influence of biogeography on trait evolution. I find little support for the traditional theory of character displacement in sympatric species. I do, however, find some support for biogeographic theories. Taken together my results do not support traditional theories on the ecological and biogeographical basis of divergence, even in those cases where Zosterops have been used as exemplars. This appears to be because those theories assume rather simple patterns of colonisation and a static ecological system. Instead, my results suggest that evolutionary diversification is dominated by recurrent waves of colonisation and extinction, which, viewed at any particular moment, tend to obscure any underlying ecological rules. 2 Declaration I declare that all the work presented in this thesis has not been previously submitted for a university degree and is entirely my own work, with the following acknowledgements: Chapter 2 Mr. H. Blaffart provided assistance with fieldwork. Dr. R. Prys-Jones and Mr. M. Adams (both Natural History Museum, Tring) provided Zosterops samples. Mr A. Krupa, Dr. G. Horsburgh (both Sheffield University) and Dr B. Bourke assisted with sequencing. Dr. A. B. Phillimore (Imperial College) provided advice on phylogenetic reconstruction and editorial input. Chapter 3 Dr. A. B. Phillimore (Imperial College) assisted with statistical tests and provided editorial input into the writing of this chapter. Chapter 4 Dr. A. B. Phillimore and Dr. G. H. Thomas (Imperial College) assisted with statistical tests and provided considerable editorial input. 3 Acknowledgements My thanks go firstly to my supervisors Ian Owens and Sonya Clegg for their patience, support and encouragement and particularly for answering e-mail at all sort of odd hours of the day and the night. In particular I’m very grateful to them for giving me the opportunity to see Zosterops inornatus and Zosterops flavifrons majuscula in the hand. I am also very grateful for all the handy tips on shark avoidance. I also owe an enormous debt of gratitude to Ally Phillimore and Gavin Thomas whose patience has possibly exceeded even that of my supervisors. Their support and advice on matters ranging from statistics to Shearer has been invaluable, especially during the writing phase. At Silwood Park I extend my gratitude to Simon Leather for all his support and for keeping me in touch with the invertebrate part of the world and Diana Anderson for help above and beyond the call of duty. I would also like to thank David Orme and Vincent Savolainen, my PRP panel, for all their help and advice and Mick Crawley for his help with statistics. Shai Meiri, Rich Grenyer, Tom Ezard, Jeff Bates, Mike Perring, Big Nick, Tania Jenkins, Eric Allan, David Orme, Alex Pigot, Márcia, Diego, Sarah, Tilly, Patricia Reader and Christine Short were among those who helped make the world a cheerier place. I would also like to thank all the members of the Silwood Cricket team for putting up with my attempts to bat so cheerfully. This project was funded by a Natural Environmental Research Council (NERC) studentship with support from the NERC-funded Sheffield Molecular Genetics facility. At Sheffield I would like to thank Andy Krupa, Gavin Horsburgh, Brian Bourke, Debs Dawson and Terry Burke for all their help and advice during my two, extended, periods of labwork. My time in Sheffield was made enjoyable by good company particularly that of Xav Harrison, Patricia Brekke, Claire Raisin, Helen Leggett, Chantimer and Maria Elena Mannarelli. Particular thanks go Ellie Davies and Alex Veitch for making sure I visited the pubs while I was in Sheffield and for stopping me from having to sleep on the streets. I would like to thank Hans Slabbekoorn for his advice and hospitality on a visit to Leiden. I thank Robert Prys-Jones and Mark Adams of the Natural History Museum at Tring for the use of museum samples and Guy Dutson for the use of his samples and for Zosterops discussions via e-mail. Thanks too to Robert Moyle for his advice on white-eyes. I have been fortunate to be able to spend time on field work in the south Pacific and I extend my thanks to the many people who helped it to happen. I owe a particular debt to the late Henri Blaffart, without whom my field work in New Caledonia might never have got started, for all his help in the field and for his hospitality and his friendship. Also in New Caledonia, Ahab, Sophie and Alissa Downer rescued me on more than one occasion when I found myself stranded. Martin Brinkert, Julien Baudat-Franceschi, Eric Clua and M. and Mme. Wiako and their family provided amazing hospitality and friendliness. My thanks go to Jean-Jérome Cassan, David Pauland and Michelle Le Bole for organising my permits to work on Grande Terre and the Loyalty Islands and the people of the islands for permission to conduct field work. In Vanuatu, my thanks to thank E. Bani, D. Kalfatak and T. Tiwok from the Vanatu Envirionment unit and the people of the islands for permission to conduct field work. My thanks to all those who helped me in the field including Jean-Charles Lepelrier, Maurice, James Black and Ruth Eastwood. Outside of work I have had tremendous help and support. In Particular I’d like to thank: Tim Owen; Jan Pritchard; Alex Stoker; Mike; Malc, Poppy, Leona and Alice; Niki, Chris, Amy and Robin; Effie and Andy; Mike, Nic and family; Nick, Jen and family; Gill, Paul and family and David Moss. John, Valerie and all the Eastwoods welcomed me into their family. My Mum and Dad were always ready with a kind word and David and James, with an insult. Ju and Mark were always on the end of the phone and I’d also like to thank my nephew William for understanding that, sometimes, I had to stop playing with trains and do some work. Finally special thanks go to my wife Ruth for keeping me calm, keeping me fed, for help in the field, for editing, for encouragement, for giving me so much to look forward to and for constant support and love. 4 Contents General Abstract ................................................................................................................... 2 Declaration ............................................................................................................................ 3 Acknowledgements ............................................................................................................... 4 Contents ............................................................................................................................... 5 List of Figures ....................................................................................................................... 9 List of Tables ...................................................................................................................... 10 Chapter 1 General Introduction ........................................................................................... 11 1.1 Speciation and divergence ........................................................................................ 11 1.2 Phylogenetic and phenotypic divergence in island birds ............................................ 13 1.3 The major themes ...................................................................................................... 14 1.3.1 Mode of Speciation ............................................................................................. 15 1.3.2 The origin and consequences of sympatry .......................................................... 19 1.3.3 Biogeographical effects on divergence ................................................................ 20 1.4 The requirements of a model system ......................................................................... 21 1.5 The family Zosteropidae ............................................................................................ 22 1.5.1 The Zosterops of the south west Pacific .............................................................. 24 1.5.2 Modes of evolution in the Zosteropidae ............................................................... 26 1.5.3 Origins
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