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Comparative Phylogeography of Three Primate Species in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia

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Comparative Phylogeography of Three Primate Species in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia Comparative phylogeography of three primate species in the Lower Kinabatangan Wildlife Sanctuary, Sabah, Malaysia MOHD. FAIRUS B. JALIL Thesis submitted for the degree of Doctor of Philosophy Biodiversity and Ecological Processes Research Group School of Biosciences, Cardiff University December 2006 UMI Number: U215944 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. Dissertation Publishing UMI U215944 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 Declaration This work has not previously been accepted in substance for any degree and is not concurrently submitted in candidature for any degree. Signed (candidate) Date STATEMENT 1 This thesis is being submitted in partial fulfillment of the requirements for the degree of PhD. Signed ........................... (candidate) Date .. STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by giving explicit references. Signed (candidate) Date STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed (candidate) Date STATEMENT 4 - BAR ON ACCESS APPROVED I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loans after expiry of a bar on accessapproved bv the Graduate Development Committee. S ig n ed .......... (candidate) Date Abstract This study investigates the population genetic structure of three primate species living in forest fragments of the Lower Kinabatangan Wildlife Sanctuary (LKWS), Sabah, Malaysia. The sanctuary is surrounded by oil palm plantations and human settlements but still retains high diversity of both flora and fauna. LKWS is famous for its orang-utan and proboscis monkey populations but also supports Sabah’s eight other primate species. The current study investigated the effects of forest fragmentation and geographical barriers, especially the Kinabatangan River, on three species of primates with different social systems and dispersal abilities. The orang-utan is a large bodied, solitary ape that is incapable of swimming whereas the proboscis monkey and the long-tailed macaque, are smaller bodied, live in large groups and are good swimmers. Using non-invasive samples (faeces), we sequenced approximately 100 individuals from each of these three primates using the left domain (and right domain for long-tailed macaques) of the mitochondrial control region. High levels of genetic diversity were detected in the proboscis monkey and long-tailed macaque, but lower levels were detected in the orang-utan. Statistical analyses (haplotype and nucleotide diversities, mismatch distributions and neutrality tests) indicate that the orang-utan and the proboscis monkey have experienced population bottlenecks, which for the orang-utan supports our earlier studies using microsatellites. Long-tailed macaques, on the other hand, show evidence of population stability. As predicted from the known mobility of these primates, the Kinabatangan River did not appear to impede the movement of proboscis monkeys and long­ tailed macaques, but did act as a geographical barrier for orang-utans. Furthermore, re­ analysis of the current data with previously published sequences of orang-utans collected throughout Borneo revealed the likely importance of rivers in differentiating between populations that corresponded closely to currently described subspecies (with the exception of the subspecies morio). There are four general conclusions from the current study. Firstly, non-invasive faecal samples are viable for large scale studies on these wild primate populations. Secondly, mitochondrial DNA is an informative marker for population studies due to its high levels of polymorphism over small spatial scales (with the left domain of the control region providing better resolution than the right domain). Thirdly, the social structure of primate species profoundly influences patterns of mitochondrial genetic diversity. Finally, dispersal patterns greatly influence the mitochondrial genetic structure of these populations. The implications of these findings for the future of Borneo primates and conservation of Lower Kinabatangan Wildlife Sanctuary and Sabah are discussed. Acknowledgements First and foremost, I would like to acknowledge the Malaysian Government and the SLAB- UMS programmes for financing my PhD in Cardiff University. I would also like to recognize the kind assistance of the Director of the Institute for Tropical Biology and Conservation, Prof. Datin Dr. Maryati Mohamed and the former Vice Chancellor, the honourable Tan Sri Prof. Datuk Seri Panglima Dr. Abu Hassan Othman for their approval of my study. I would also like to acknowledge the support of the current Vice Chancellor, the honourable Prof. Dato’ Dr. Mohd. Noh Dalimin. I am really grateful to all my supervisors, Prof. M.W.Bruford, Dr. J. Cable and Dr. B. Goossens, for all their guidance, assistance and patience during my study at Cardiff University and in Kota Kinabalu. I am also grateful to Dr. M. Ancrenaz, Dr. I. Lackman- Ancrenaz and Assoc. Prof. Dr. M. Schilthuizen for their help throughout the project. Many people helped me throughout my years here in Cardiff my ‘G10/11 family University. The G10 lab that has been my home for the past 3 years and particularly, Gabby, Rhys, Simon, Patricia, Elis, Sofia, Mirrerid, Angela, David, Mireille, Kath D, Geoff, Tim and Jorge, that provided comfort and laugh, and kept me sane throughout the years in Cardiff. The Oracles o f G10, Yoshan, Amy, Andy, Carlos, Trini, Erica, Sam, for instant guidance in the many facets of lab work and analyses. In Malaysia, I would like to acknowledge the kind assistance of Sabah Wildlife Department, the members of Kinabatangan Orang-utan Conservation Project and Institute for Tropical Biology and Conservation, UMS for their kind assistance during my time collecting samples and going through all the formalities of studying abroad. Also, for my assistance Jamil Sinyor, thank you for accompanying me on many difficult and tedious sampling trips. This thesis is dedicated to my family and the people of Kinabatangan and their effort to save and protect the area... Table of Contents Declaration ii Abstract iii Acknowledgements iv Table of Contents V List of Tables vii List of Figures ix Chapter 1: Introduction 1 1.1 Historical biogeography of South East Asia 1 1.2 Tropical rainforest and deforestation 5 1.2.1 Logging 6 1.2.2 Agriculture 7 1.2.3 Forest fires 7 1.2.4 Impact of deforestation on biodiversity in Borneo 8 1.3 Primates of Sundaland 9 1.3.1 The orang-utan 10 1.3.2 The long-tailed macaque 14 1.3.3 The proboscis monkey 16 1.4 Phylogeography and conservation genetics 18 1.5 Molecular markers 19 1.5.1 mtDNA 19 1.5.2 Microsatellites 21 1.6 Non-invasive samples for endangered mammals 21 1.7 The Lower Kinabatangan Wildlife Sanctuary 24 1.8 Aims 26 Chapter 2: Material & methods 29 2.1 Sampling 29 2.1.1 Section 1 (Lots 1 and 2) 30 2.1.2 Section 2 (Lots 5, 6 and 7) 32 2.1.3 Section 3 (Lots 3 and 4) 33 2.1.4 Section 4 (Lots 8, 9 and 10) 34 2.2 Genetic studies 35 2.2.1 Faecal DNA extraction protocol 35 2.2.2 Hair extraction protocol 36 2.2.3 Standard PCR protocol 37 2.2.4 DNA sequencing 38 2.3 Data analysis 39 2.3.1 Sequence alignment and editing 39 2.3.2 Genetic diversity 39 2.3.3 Analysis of molecular variance (AMOVA) 40 2.3.4 Networks 41 2.3.5 Mismatch distributions 42 2.3.6 Selective neutrality 43 2.3.7 Coalescent simulation 43 Chapter 3: Mitochondrial genetic structure of the long-tailed macaque (Macaca fascicularis) in the Kinabatangan Floodplain, Sabah, Malaysia. 44 Abstract 44 3.1 Introduction 44 3.2 Material and methods 47 3.3 Results 51 3.4 Discussion 60 Chapter 4: Rivers influence the population genetic structure of Bornean orang-utans (Pongo pygmaeus) 69 Abstract 69 4.1 Introduction 69 4.2 Material and methods 71 4.3 Results 76 4.4 Discussion 88 Chapter 5: Genetic structure and dispersal in a proboscis monkey (Nasalis larvatus) population in Sabah, Malaysia. 97 Abstract 97 5.1 Introduction 97 5.2 Material and methods 100 5.3 Results 104 5.4 Discussion 111 Chapter 6: Final discussion 117 6.1 Historical perspectives on colonization 118 6.2 Primate population demography 122 6.3 Impact of rivers on primates 127 6.4 Influences of ox-bow lakes 128 6.5 Food competition 129 6.6 Social behaviour influences population structure 130 6.7 Conservation issues for Kinabatangan Primates 131 Future directions 133 References 135 Appendix I 152 Appendix II 153 Appendix III 169 Appendix IV 181 VI List of Tables Table Page 2.1 Fieldwork timetable (dry season June to July and rainy season August to 30 September) 2.2 Species-specific PCR primers developed and used for this study. 38 2.3 Grant & Bowen’ (1998) interpretation of differences between haplotype and 40 nucleotide diversities. 3.1 Variable nucleotide positions in the alignment of mtDNA sequences of the 52 long-tailed macaque control region. Dots indicate positions where the bases are identical to haplotype LD01. 3.2 Haplotypes of left domain (LD) of mtDNA control region observed for 53 long-tailed macaques and their frequency in each Lot and forest reserve.
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