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Phylogeny and Biogeography of Gibbons, Genus Hylobates

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Phylogeny and Biogeography of Gibbons, Genus Hylobates Phylogeny and Biogeography of Gibbons, Genus Hylobates. by Helen Jane Chatterjee Department of Biology, University College London A thesis submitted for the fulfilment of the Degree of Doctor of Philosophy University of London, 2000 ProQuest Number: U643055 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest. ProQuest U643055 Published by ProQuest LLC(2016). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. Microform Edition © ProQuest LLC. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 A bstract This thesis aims to reconstruct the phylogenetic and biogeographic history of gibbons, genus Hylobates. Phylogenetic relationships among gibbons are controversial. This study uses molecular and morphological data to resolve some of these controversies, and provides a new phylogeny for the genus. The estimate of gibbon phylogeny is combined with distribution data to reconstruct the biogeographic history of gibbons. In the first part of the study, original mitochondrial control region sequence data and published cytochrome b gene sequence data are analysed using maximum likelihood, parsimony and bootstrapping methods. Results of these analyses indicate a gibbon phylogeny which shows the following subgeneric relationships: Nomas eus, Symphalangus and Bunopithecus are successively more closely related to Hylobates. A molecular clock is employed which suggests that the gibbon radiation dates to about 10.5 million years ago (Ma). In the second part of the study, craniodental and postcranial metric variables are analysed using multivariate statistical methods to investigate interspecific morphological variability. Multivariate statistical analyses across the gibbon skeleton show that the eleven currently recognised species form five distinct morphological groups. The metric data are further employed to investigate phylogenetic inter­ relationships among gibbons. These data are converted into discrete character states using segment and range coding. The re-coded data are analysed using parsimony and bootstrapping methods. These analyses indicate that gibbon skeletal metric data is phylogenetically uninformative at the species or subgenus level. In the third part of the study, three alternative methods of biogeographic reconstruction are employed: ancestral area analysis using irreversible parsimony, ancestral area analysis using reversible parsimony and dispersal-vicariance analysis (DIVA). Results of the DIVA analysis are combined with estimates of divergence dates, to propose a new pattern of radiation for the genus Hylobates. This analysis indicates that the gibbon radiation may have begun in Indochina around 10.5 Ma. Between 10.5 and 8.6 Ma gibbons radiated southwards to Sumatra. Subsequently, they differentiated into two types of gibbon on Sumatra, representing the subgenera Symphalangus and Hylobates. A third radiation approximately 7-8 Ma saw the dispersal of Bunopithecus into Burma, Assam, and Bangladesh. At around 3-5 Ma there was a second radiation of subgenus Hylobates, involving dispersal onto the islands of Borneo, Mentawai and Java. Between 0.3 and 1.8 Ma taxa in the subgenus Nomascus differentiated into Cambodia and Hainan Island. This study provides a novel reconstruction of the historical biogeography of gibbons. In addition, parsimony and likelihood analyses of molecular and morphological data sheds light on the controversial topic of hylobatid phylogeny. Acknowledgements I am indebted to my two supervisors Professor Leslie Aiello and Dr. Adrian Lister, for their unceasing support and encouragement, for their patience and guidance, and their enthusiasm. I am most sincerely grateful to Dr. Mark Collard and Dr. Mark Thomas for their teaching, time, and guidance. I wish to also acknowledge Dr Mark Thomas and Neil Bradman for giving me the opportunity to work in their laboratory. I am grateful to University College London (especially the Department of Biology) not least for their financial support, but also for giving me the opportunity to work in The Grant Museum of Zoology. The following people and institutions were especially generous in providing samples for the genetic part of this study: Dr. Malcolm Hall, formerly of the University of Liverpool. Dr. Ann Oakenfull, Department of Genetics, University of Cambridge, Dr. Volker Sommer, Department of Anthropology University College London, Dr. Andrew Kitchener, National Museums of Scotland, Marwell Zoo, UK, Twycross Zoo, UK, and the Mammals Section, Department of Zoology, British Museum of Natural History, London. I would like to say a special thank you to Malcolm Hall for his generous gift of numerous gibbon hair samples, his encouragement and several interesting discussions. I wish to thank Curators from the following Museums for providing access to their fantastic gibbon collections: the Natural History Museum, London (United Kingdom), the Rijksmuseum van Natuurlijke Histoire, Leiden (The Netherlands), the American Museum of Natural History, New York (United States of America), the Field Museum of Natural History, Chicago (United States of America), and the National Museum of Natural History, Smithsonian Institute, Washington DC. (United States of America), and the Department of Anatomy, UCL (UK). For exchange of correspondence and/or discussions, plus much useful information, I would like to thank Drs. Colin Groves, Nina Jablonski, Ian Barnes, Doug Brandon-Jones and Marcello Ruta. I am especially grateful to Dr. Marcello Ruta for his time, teaching and encouragement. For numerous lively discussions, unceasing support and encouragement I wish to thank the following friends and colleagues: Paul Davies, Sarah Collinge, Margaret Clegg, Julia Day, Marcello Ruta, Sam Cobb, Claire Imber, Helen Wood, Will Harcourt- Smith, Hartley Odwak; plus, Jo, Gillie, Louise, Karen, Maya and everyone in the Department of Biology who has given me support and many kind words. I also wish to thank all of my friends outside of work who have provided fun, support and encouragement. There are many others to whom I am grateful for help, support and discussion, who are too numerous to mention; I am thankful to everyone who has helped me. Finally, I am grateful to my family: Martin, Betty, Nan, Ranjit, Andrew, Ashraf, Kumie, Shakeeb, Leyya, Zoë, Shanta and Ryan. Without their encouragement, commitment, love and moral support, I could not have completed this. Phylogeny and Biogeography of Gibbons, Genus Hylobates, Contents Page Numbers Title 1 A bstract 2 Acknowledgements 3 Contents 5 List of figures and tables 8 Chapter 1: Introduction and Background 15 1.1 Aims and objectives 16 1.2 Structure of the thesis 18 1.3 Gibbon systematics, evolution and geographic distribution 19 1.3.1 Introduction to gibbon systematics 19 1.3.2 Historical background to gibbon systematics 20 1.3.3 Geographic distribution of gibbons 27 1.3.4 Palaeontological and palaeoenvironmental background 36 1.4 Background to previous studies 45 1.4.1 Review of previous molecular studies 48 1.4.2 Review of previous morphological studies 56 1.4.3 Review of previous biogeographic studies 64 1.5 Summary 71 Chapter 2: Molecular Study 72 2.1 Introduction and background to study 73 2.1.1 The mitochondrial control region 75 2.1.2 Mitochondrial cytochrome b gene 77 2.2 Materials and methods 79 2.3 Phylogenetic analysis 85 2.4 Phylogenetic results and discussion 89 2.5 Conclusions 123 Chapter 3: Morphological Study 124 3.1 Introduction 125 3.2 Materials 126 3.3 Measurements 130 3.4 Methods of analysis 148 3.4.1. Multivariate statistical methods 148 3.4.2 Multivariate statistical results and discussion 154 3.4.3 Cladistic methods 192 3.4.4 Cladistic results and discussion 202 3.5 Conclusions 225 Chapter 4: Biogeographic Study 227 4.1 Introduction to Historical Biogeography 228 4.1.1 Dispersal Biogeography 231 4.1.2 Panbiogeography 232 4.1.3 Vicariance Biogeography 233 4.1.4 Cladistic Biogeography 234 4.1.5 Alternative biogeographic models - Réfugia 237 4.2 Materials and Methods 239 4.2.1 Ancestral area analysis using irreversible parsimony 244 4.2.1.1 Introduction to the method 244 4.2.1.2 The method 244 4.2.1.3 Results 247 4.2.2 Ancestral area analysis using reversible parsimony 248 4.2.2.1 Introduction to the method 248 4.2.2.2 The method 248 4.2.2.3 Results 250 4.2.3 Dispersal-vicariance analysis 252 4.2.3.1 Introduction to the method 252 4.2.3.2 The method 253 4.2.3.3 Results 259 4.3 Discussion 261 4.4 Conclusions 268 Chapter 5: Final discussion, conclusions and future research 269 5.1 Final discussion 270 5.1.1 Molecular approach to gibbon phylogeny 271 5.1.2 Morphological study 274 5.1.3 Gibbon biogeography 277 5.2 Concluding remarks 282 5.3 Future research 284 Appendices 286 Appendix I. Pelage Descriptions 287 Appendix II. Control Region sequence data 294 Appendix III. Segment and Range coded metric data matrices 296 Appendix IV. Non size-corrected (raw) cranial, dental and postcranial data 308 References 338 List of figures and tables Figures Figure 1.1 Map of Southeast Asia ............................................................................................. 30 Figure 1.2 Distribution of gibbon subgenera, after
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