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Radiation and Macroevolutionary Ecology of the African Genus Protea L

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Radiation and Macroevolutionary Ecology of the African Genus Protea L. Gail Reeves A thesis submitted for the degree of Doctor of Philosophy Imperial College of Science, Technology and Medicine & NERC Centre for Population Biology University of London January 2001 1 Abstract The Cape floristic region (CFR) of South Africa harbors one of the highest concentrations of plant species on Earth. The aim of this thesis was to investigate factors promoting the radiation of this diverse flora using a reconstructed species-level molecular phylogeny for one of the CFR's flagship genera, Protea. Chapter 2 of this thesis describes the use of five non-coding regions from the plastid and nuclear genome to reconstruct relationships among 88 Protea species. Extremely low levels of sequence divergence were found among species, and consequently in Chapter 3 amplified fragment length polymorphism (AFLP) markers were also employed to infer relationships. These markers were found to be extremely useful in combination with DNA sequence data for phylogenetic reconstruction in this group. Contrary to previous hypotheses, the phylogeny supports a Cape origin for the group followed by expansion into tropical Africa. In Chapter 4, the age of the root node of Protea was estimated to evaluate the widely held view that much of the diversification in the Cape occurred since the onset of Mediterranean-type climates ca. five million years ago. Contrary to this hypothesis, the timing and the temporal dynamics of the radiation of Protea indicated that the lineage is at least 36 myr old, and that its diversification rate has declined significantly over the last 20 mya. Chapter 5 investigates the role of special characteristics of the CFR, including complex topography and heterogenous edaphic environment in the diversification of the flora. In Protea, it appears that speciation has been largely allopatric, but there is no significant pattern to suggest that soil factors or habitat subdivison have been involved in speciation. Comparison of diversification rates between lineages that re-seed and re- sprout after fire indicated higher diversification rates in the former within the Cape, but this rate is less than that for re-sprouting lineages outside of the Cape. In summary, the diversity of Protea species in the CFR may be due to high coexistence of species that diversified over a long timespan, rather than a recent rapid radiation in this lineage. 2 Acknowledgements As possibly the most extensively supervised PhD student in the history of PhD students I have a considerable list of those to whom I owe enormous gratitude. At Imperial College and the NERC Centre for Population Biology my supervisors Tim Barraclough, John Lawton and Alfried Vogler, also CPB staff Phil Heads and Claire Challis. At the Royal Botanic Gardens, Kew my advisors Mark Chase and Mike Fay, also staff of the Molecular Systematics section Vincent Savolainen, Cassio Van den Berg, Robyn Cowan, Jeff Joseph, Martyn Powell and Tim Fulcher. In Cape Town our collaborators at the National Botanical Institute Tony Rebelo and John Rourke, and at the Institute for Plant Conservation UCT, Richard Cowling. Also in South Africa Mervyn Lotter, Wendy Paisley, Suzette Foster, my beautiful field assistant Stephanie Yelenick and all those involved in the Protea Atlas Project, especially Nigel Forshaw and Val Charlton. Extra special personal thanks go to: my surrogate family - the Cherries, M & M, private programmer Rob, fishing-partner Andrew and best friends Emma, Sarah and Anouk. Finally, my forever-supportive family: Nan, Grandma, brother Ben, soon-to-be-husband Steve, and most of all Mum and Dad. 3 Table of Contents Abstract 2 Acknowledgements 3 Table of Contents 4 Index of Figures 7 Index of Tables 11 Chapter One - General Introduction 13 D Physical and ecological setting 14 D Causes of species richness 16 D Reconstructed phylogenies as tools for studying diversification 17 D Protea as a case study 18 Chapter Two - Molecular Phylogenetics of Protea: Evidence from Plastid and Nuclear DNA Sequences 24 Materials and Methods 26 Results 34 D ITS region 34 D Plastid regions 34 D ncpGS region 35 D Plastid and ncpGS regions combined 36 Discussion 46 Chapter Three - Phylogenetic Reconstruction of Protea: Combined Evidence from DNA Sequence Data and AFLP Markers 50 Materials and Methods 54 Results 60 D AFLPs 60 D AFLP and DNA sequence data combined 60 4 Discussion 70 Chapter Four - Timing and Temporal Dynamics of the Radiation of Protea 72 Materials and Methods 76 > Age estimation for the root node of the Protea clade 76 D Producing an ultrametric tree 76 > Temporal dynamics of the radiation of Protea 77 Results 83 > Age estimation for the root node of the Protea clade 83 D Temporal dynamics of the Protea radiation 85 Discussion 95 D Sources of error in age estimates 95 > Use of the correct tree and substitution noise 95 D Incorrect calibration 96 > Variability in substitution rate 96 > Age estimate for the radiation of Protea and its implications 97 D Temporal dynamics of the Protea radiation 97 Chapter Five — Investigating the Factors Promoting Diversification in Protea using Sister Group Analysis 99 > Topography 99 > Edaphic specialization 100 > Fire 102 Materials & Methods 103 > Topography 103 > Edaphic specialization 104 D Relationship between habitat preference and degree of sympatry 105 > Fire survival strategy 105 Results 108 > Topography 108 > Edaphic Specialization 108 > Relationship between sympatry and habitat difference 110 D Diversification rate in re-seeding and re-sprouting lineages 111 Discussion 116 D Topography 116 5 > Edaphic specialization 116 > Fire 117 > Summary 118 Chapter 6 - Conclusions 120 References 124 APPENDIX 1 CD ROM affixed to back cover > PAUP file 1: DNA sequence and AFLP matrices used in Chapters 2 & 3 > PAUP file 2: DNA sequence matrix used in Chapter 4, analysis 1 > PAUP file 3: DNA sequence matrix used in Chapter 4, analysis 2 6 Index of Figures Chapter 1 FIGURE 1 14 Distribution of fynbos within the CFR (after Low & Rebelo 1998). FIGURE 2 22 Geological time-scales and sequence of some of the important events in the history of the fynbos region (after Deacon et al. 1992 & Cowling & Richardson 1995). FIGURE 3 19 Geographical distribution of Protea throughout Africa (after Rourke 1980). FIGURE 4 .21 WorldMap (Williams 1998) representation of Protea species diversity in the CFR. Grid cells are 1/8 degrees on a side —12Icm. Colour scale indicates Protea species diversity of zero to a maximum of 23. (Reproduced with kind permission of the Trotea Atlas Project', National Botanical Institute, Cape Town.) Chapter 2 FIGURE 1 38 One of the equally most parsimonious trees found from analysis of ITS sequences for 14 Protea and one Faurea species. Number of trees = 96, number of steps = 548, CI = 0.76, RI = 0.80. Branches not recovered in the strict consensus are indicated with a circle. Branches lengths are shown above and bootstrap percentages below the branches. Terminal taxa with identical names were sequenced from the same plant. FIGURE 2 39 Adams consensus of 9490 equally most parsimonious trees found from analysis of four plastid DNA non-coding regions for 88 species of Protea. Number of steps = 238, CI = 0.84, RI = 0.91. Branches not recovered in the strict consensus are indicated with a circle. Bootstrap percentages are indicated below branches. FIGURE 3 40 Adams consensus of 3280 equally most parsimonious trees found from analysis of ncpGS sequences for 77 Protea species. Branches not recovered in the strict consensus are indicated with a circle. Bootstrap percentages are indicated below the branches. FIGURE 4 41 One of the equally most parsimonious trees found in the combined analysis of ncpGS and plastid data sets. Branch lengths are shown above branches. Indels scored from both data sets are indicated on the tree. Taxa in bold are found in summer rainfall regions. FIGURE 5 42 Adams consensus of one of the 3280 equally most parsimonious trees found in the combined analysis of ncpGs and plastid data sets. Number of steps = 514, CI = 0.82, RI = 0.89. Branches not recovered in the strict consensus are indicated with a circle. Bootstrap percentages are indicated below branches. 7 Figure 6 48 (a) hypothetical phylogenetic reconstruction of the relationship among tropical and Cape taxa according to Rourke (1998). (b) relationship among tropical and Cape Protea species recovered in the DNA sequence trees. Chapter 3 FIGURE 1 .53 Schematic of the AFLP procedure. FIGURE 2 .62 Adams consensus of 26 equally most parsimonious trees found from analysis of 138 AFLP bands for 72 Protea taxa. Number of steps = 609, CI = 0.23, RI = 0.52. Branches not recovered in the strict consensus are indicated with a circle. Bootstrap percentages are indicated below branches. FIGURE 3 .63 Rooted neighbour joining phylogram derived from analysis of 138 AFLP bands for 72 Protea taxa. FIGURE 4 .64 One of the 20 equally most parsimonious trees found in a combined analysis of DNA sequence and AFLP data sets. Branch lengths are indicated above the branches. FIGURE 5 .65 Adams consensus of 20 equally most parsimonious trees found in a combined analysis of DNA sequence and AFLP data sets for 86 Protea species. Number of steps = 1185, CI = 0.47, RI = 0.65. Branches not recovered in the strict consensus are indicated with a circle. Bootstrap percentages are indicated below branches. FIGURE 6 66 Major clades recovered from analysis of (a) DNA sequence, (b) AFLP and (c) combined data sets. Taxonomy corresponding to the numbered clades is detailed in Table 2. * corresponds to taxa that are missing from a clade with respect to those identified in 6c. Groups that are not recovered in the strict consensus are marked with a circle. Figure 7 67 Percentage of missed homoplasy discovered for subsets of informative characters with respect to the best tree built from 302 characters (curve A) and 150 characters (curve B).
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