Range-wide chloroplast DNA phylogeographies of three widespread Australian cool temperate rainforest plants
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1 Range-wide chloroplast DNA phylogeographies of three widespread Australian cool temperate rainforest plants by James Raymond Peter Worth, BSc (Hons). Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy University of Tasmania (November, 2009)
2 i Declarations This thesis does not contain any material which has been accepted for a degree or diploma by the University of Tasmania or any other institution. To the best of my knowledge and belief this thesis contains no material previously published or written by another person except where due acknowledgment is made in the text of the thesis. James R. P. Worth This thesis may be made available for loan and limited copying in accordance with Copyright Act James R. P. Worth
3 ii Abstract How temperate plants and animals survived hostile climates during past glacial periods is critical to understanding modern ecological communities. Species may have survived in macro-refugia, and migrated large distances to reach their current range since climates recovered 10-12,000 years ago, or may have survived in many micro-refugia. The cool temperate rainforest of southeastern Australia provides opportunities to better understand how these processes have shaped the current biota. This thesis investigates the range-wide chloroplast DNA phylogeographies of three widespread Australian cool temperate rainforest plants. In the gravity-dispersed tree, Nothofagus cunninghamii (Nothofagaceae), 23 haplotypes were identified by PCR-RFLP and sequencing of 2164 base pairs of chloroplast DNA from 342 individuals. Deep haplotype divergence occurred, with the haplotype of N. moorei nested among those of N. cunninghamii. Western Tasmania was the stronghold of haplotype diversity, with evidence for multiple glacial refugia in coastal and inland locations. Three haplotypes endemic to the Victorian Central Highlands corroborate pollen evidence for last glacial maximum survival. In eastern Tasmania, an endemic and deeply diverged haplotype suggests long-term occupation within this region. In the bird-dispersed shrub Tasmannia lanceolata (Winteraceae) 30 haplotypes were identified by sequencing of 3190 base pairs of chloroplast DNA from 244 individuals. Strong phylogeographic structuring, with eight clades with predominantly nonoverlapping geographic distributions, provided evidence for multiple glacial refugia, including within the driest parts of the species range. This strong structure may be the result of the lack of vectors for effective long-distance dispersal, such as migratory birds. However, other factors limiting establishment at long distances, such as dioecy, competition, or selection may have contributed. Sequences of 3295 base pairs from 142 samples of the wind-dispersed tree, Atherosperma moschatum (Atherospermataceae), revealed low chloroplast variation (six haplotypes). The apparently ancestral haplotype was widespread across Tasmania. A single haplotype was found across all Victorian populations, while the most diverged haplotypes were observed near the northern limit of the species range in New South Wales.
4 iii The deep phylogeographic patterns in N. cunninghamii and T. lanceolata are the result of probable long-term survival in multiple regions, indicating the resilience of these species in apparently hostile last glacial climates. Differing dispersal traits have not affected the limited mobility of these species in response to past climatic changes. This contrasts with the extensive continent wide migrations of temperate species in the northern hemisphere. However, the very low diversity in A. moschatum may indicate a divergent history of this species.
5 Acknowledgements I would like to thanks my supervisors Greg Jordan and René Vaillancourt who have been so patient and supportive throughout this work. I would like to thank them both for teaching me so much, and there useful insights that improved this project. I would also like to thank my research supervisor Gay McKinnon for assistance with phylogenetic techniques. This project would have taken far longer without some help in the field and in the lab. I would specifically like to thank Adam Smolenski for his fantastic help in the lab when things weren't working and James Marthick who was gave invaluable assistance in the lab and field and showed great enthusiasm for this project. Many people helped me out by collecting samples including J and N Cross (King Island), Greg Dutkowski, Taylor Feild, Dave Handscombe (Parks Vic), Corey Hudson, Jasmine Janes, Sue Jennings, Rebecca Jones, Anthony Mann, Jon Marsden-Smedley, Trevor McIntosh (Parks Vic), Simon Whittock and Dave Woods (Parks NSW). I also acknowledge the useful advice and discussions I had at times with Tim Brodribb, Bob Elliot, Des Fitzgerald, Jules Freeman, Robert Mesibov and Dorothy Steane. I would like to thank my parents who were gave me a place to live throughout most of this work and Ray Worth was a great help during field trips in Tasmania. Lastly, I would like to thank Madoka for her support, patience and encouragement while I undertook this work. iv
6 v Publications from this thesis Refereed articles Worth, JRP, Jordan, GJ, McKinnon, GE and Vaillancourt, RE The major Australian cool temperate rainforest tree Nothofagus cunninghamii withstood Pleistocene glacial aridity within multiple regions: evidence from the chloroplast. New Phytologist 182: Conference articles Worth, JRP, Vaillancourt, RE, Jordan, GJ, McKinnon, GE Chloroplast DNA reveals genetic legacy of ice ages in the rainforest species Nothofagus cunninghamii. In Proceedings of 'Old Forests, New Management' Sir Mark Oliphant Conference, February 2008, Hobart, Australia. p. 67. Worth, JRP, Vaillancourt, RE, Jordan, GJ Where did Nothofagus cunninghamii survive the ice ages? In Proceedings of 'Australasian Quaternary Association', 2004, Cradle Mountain, Australia. p. 43.
7 vi Table of contents DECLARATIONS... I ABSTRACT... II ACKNOWLEDGEMENTS... IV PUBLICATIONS FROM THIS THESIS... V CHAPTER 1: INTRODUCTION... 1 General introduction... 1 The fossil record... 2 The molecular approach... 3 Problem Statement... 4 Cool temperate rainforest of southeastern Australia- a model system... 5 This thesis Structure of this thesis CHAPTER 2: THE MAJOR AUSTRALIAN COOL TEMPERATE RAINFOREST TREE NOTHOFAGUS CUNNINGHAMII WITHSTOOD PLEISTOCENE GLACIAL ARIDITY WITHIN MULTIPLE REGIONS: EVIDENCE FROM THE CHLOROPLAST...18 INTRODUCTION MATERIALS AND METHODS The study species Sampling Molecular methods Phylogenetic relationships of haplotypes Spatial clustering and regional haplotype diversity RESULTS cpdna variation and phylogenetic relationships Distribution, spatial clustering and regional haplotype diversity Northeast highlands haplotype fine-scale study DISCUSSION Antiquity of haplotypes Western Tasmania: the major reservoir of chloroplast diversity Molecular evidence for glacial refugia outside regions of expected survival The widespread subclade and Victorian populations Conclusions APPENDICES Appendix Appendix Appendix CHAPTER 3: STRONG PHYLOGEOGRAPHIC STRUCTURE OF THE BIRD-DISPERSED SHRUB TASMANNIA LANCEOLATA (WINTERACEAE)...51 INTRODUCTION MATERIALS AND METHODS Species description Sampling strategy Molecular methods Test for neutrality and spatial structuring... 59
8 Phylogenetic estimation of cpdna haplotypes RESULTS Chloroplast variation Phylogenetic relationships of Tasmannia Strong phylogeographic structuring of T. lanceolata haplotypes DISCUSSION Chloroplast evidence for short-range dispersal Evidence for the dominance of short-range dispersal The difficulty of establishing new populations The possible role of selection Other implications Conclusions APPENDICES Appendix Appendix CHAPTER 4: CHLOROPLAST PHYLOGEOGRAPHY OF THE WIND-DISPERSED COOL TEMPERATE RAINFOREST TREE ATHEROSPERMA MOSCHATUM (ATHEROSPERMATACEAE)...90 INTRODUCTION MATERIALS AND METHODS The study species Sampling Molecular methods DNA sequence and haplotype analysis Phylogenetic analysis RESULTS PCR-RFLP DNA Sequencing Phylogenetic relationships and distribution of haplotypes Nucleotide diversity and tests for selection DISCUSSION Low chloroplast variation Towards an explanation of low diversity in A. moschatum Biogeographic implications The northern populations APPENDICES Appendix Appendix CHAPTER 5: PRELIMINARY INVESTIGATION OF CHLOROPLAST VARIATION IN THREE TASMANIAN ENDEMIC COOL TEMPERATE RAINFOREST PLANTS: OLEARIA PERSOONIOIDES (ASTERACEAE), PHYLLOCLADUS ASPLENIIFOLIUS (PODOCARPACEAE) AND TELOPEA TRUNCATA (PROTEACEAE) INTRODUCTION MATERIALS AND METHODS Study species Sampling Molecular Methods RESULTS AND DISCUSSION Olearia persoonioides- PCR/RFLP vii
9 Olearia persoonioides- DNA sequencing Phyllocladus aspleniifolius-pcr/rflp Phyllocladus aspleniifolius-dna sequencing Telopea truncata-pcr-rflp Telopea truncata-dna sequencing CHAPTER 6: CONCLUSIONS Outline of discussion The roles of adaptation and tolerance in the history of southern cool temperate rainforests Limited mobility during the Holocene Antiquity of haplotypes and geographic patterns of haplotypes REFERENCES viii
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