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The Phylogeny and Evolution of Two Ancient Lineages of Aquatic Plants

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The Phylogeny and Evolution of Two Ancient Lineages of Aquatic Plants The Phylogeny and Evolution of Two Ancient Lineages of Aquatic Plants by William James Donaldson Iles B.Sc., The University of Toronto, 2005 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate Studies (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) May 2013 c William James Donaldson Iles 2013 Abstract In my thesis I aim to improve our phylogenetic and evolutionary knowledge of two ancient and distantly related groups of aquatic flowering plants, Hy- datellaceae and Alismatales. While the phylogeny of monocots has received fairly intense scrutiny for two decades, some parts of its diversification have been less frequently investigated. One such lineage is the order Alismatales, which defines one of the deepest splits in monocot evolution. Many fami- lies of Alismatales are aquatic or semi-aquatic, and they have been impli- cated in historical discussions of monocot origins. I evaluate inter-familial relationships in the order, considering a suite of 17 plastid genes for 31 Al- ismatales taxa for all 13 recognized families. This study improves on our understanding of, and confidence in, higher-order Alismatales relationships. I also uncovered convergent gene loss of plastid-encoded subunits for the NADH dehydrogenase complex. I then expand monocot coverage outside Alismatales by including unpublished and newly sequenced data for other orders. This large-scale sample facilitated a re-evaluation of monocot phy- logeny and molecular dating, the latter using 25 fossil constraints. Previ- ously included in the monocot order Poales, Hydatellaceae are a small family of ephemeral aquatics relatively recently found to be the sister group of wa- ter lilies (Cabombaceae and Nymphaeaceae). I present the first molecular phylogeny of the family and evaluate aspects of the family's morphological evolution. I show how sexual system shifts are associated with shifts in other reproductive traits. I also infer a temporal scale for Hydatellaceae diversifi- cation using a two-step Bayesian approach. I use the resulting dated tree to address biogeographic patterns and aspects of niche evolution. I show that its \Gondwanan" distribution is the result of long-distance dispersal and not continental rifting, and demonstrate strong phylogenetic niche conser- ii vatism in the family. These studies expand our understanding of evolution in Hydatellaceae, and provide a substantial update to our understanding of Alismatales (and more generally monocot) phylogeny and divergence times. iii Preface All chapters benefited from input from coauthors. A version of Chapter 2 was previously published as: Iles W.J.D., Rudall P.J., Sokoloff D.D., Remizowa M.V., Macfar- lane T.D., Logacheva M.D., and Graham S.W. 2012. Hydatel- laceae (Nymphaeales): sexual-system homoplasy and a new sec- tional classification. American Journal of Botany 99: 663{676. I produced most of the sequence data, carried out analysis, and wrote the manuscript. P.J. Rudall, D.D. Sokoloff, M.V. Remizowa and T.D. Mac- farlane collected and provided plant material. M.D. Logacheva produced a small amount of sequence data. D.D. Sokoloff and M.V. Remizowa did character scoring and measurements. D.D. Sokoloff produced the sectional treatment. S.W. Graham conceived of the initial project and provided guid- ance. All authors helped with writing and editing. Chapter 3 was coauthored. I conceived of the initial project, carried out most of the analyses, and wrote most of the manuscript. D.D. Sokoloff, M.V. Remizowa, S.R. Yadav, M.D. Barrett, R.L. Barrett, and T.D. Macfar- lane provided accession location data for georeferencing. C. Lee carried out georeferencing and Maxent analysis, and wrote an initial draft of the corre- sponding material and methods section. S.W. Graham helped with writing and provided guidance. All authors helped with editing. A version of Chapter 4 is in press as: Iles W.J.D., Smith S.Y., and Graham S.W. In press. A well- supported phylogenetic framework for the monocot order Alis- matales reveals multiple losses of the plastid NADH dehydroge- nase complex and a strong long-branch effect. P. Wilkin and S.J. Mayo [eds]. In Early Events in Monocot Evolution. Cambridge: iv Cambridge University Press. pp. 1-28. I produced most of the new sequence data (19 taxa), carried out analysis, and wrote the manuscript. S.Y. Smith produced new sequence data for six taxa. S.W. Graham conceived of the project and provided guidance. All authors helped with editing. Chapter 5 was coauthored. I conceived of the initial project, gener- ated sequence data for 12 new taxa, carried out analysis, and wrote the manuscript. J. Zgurski generated most of the new sequence data in the or- der Liliales. J.M. Saarela generated most of the new sequence data in the order Poales. G. Ross and Q. Lin each generated data for one new taxon. S.Y. Smith provided advice on fossil selection. S.W. Graham helped with writing, editing, and guidance. v Table of Contents Abstract ................................. ii Preface .................................. iv Table of Contents ............................ vi List of Tables .............................. ix List of Figures .............................. x Acknowledgements ........................... xi Dedication ................................ xii 1 Introduction ............................. 1 1.1 Water lilies and Hydatellaceae . 2 1.2 Alismatales and monocots . 4 1.3 Overview of the thesis . 9 2 Phylogenetics and sexual-system evolution of Hydatellaceae 11 2.1 Summary . 11 2.2 Introduction . 12 2.3 Materials and methods . 16 2.3.1 Taxonomic and genomic sampling . 16 2.3.2 Extraction, amplification and sequencing . 17 2.3.3 Alignment and gene-tree analyses . 18 2.3.4 Species-tree inference . 20 2.3.5 Ancestral character states and character associations 21 2.4 Results . 22 2.4.1 Plastid and nuclear phylogenies of Hydatellaceae . 22 2.4.2 Species phylogeny of Hydatellaceae . 23 2.4.3 Ancestral character-state reconstructions . 25 2.4.4 Phylogenetic ANOVAs . 28 vi 2.5 Discussion . 30 2.5.1 Gene and species phylogenies . 30 2.5.2 New classification . 32 2.5.3 Morphological evolution . 34 2.5.4 Sexual-system evolution . 35 2.5.5 Conclusions . 38 3 Biogeography and niche conservatism in Hydatellaceae . 39 3.1 Summary . 39 3.2 Introduction . 40 3.3 Material and methods . 41 3.3.1 Molecular dating . 41 3.3.2 Biogeographic reconstruction . 42 3.3.3 Climate niche evolution . 43 3.4 Results and discussion . 46 3.4.1 The age of Hydatellaceae . 46 3.4.2 Biogeography of Hydatellaceae . 49 3.4.3 Phylogenetic niche conservatism in Hydatellaceae . 50 4 Phylogeny and gene loss in Alismatales . 56 4.1 Summary . 56 4.2 Introduction . 57 4.3 Material and methods . 59 4.3.1 Taxon sampling . 59 4.3.2 Gene sampling . 60 4.3.3 Data assembly . 61 4.3.4 Phylogenetic analysis . 62 4.4 Results . 63 4.4.1 The phylogenetic backbone of Alismatales . 63 4.4.2 Taxon density and branch support . 68 4.4.3 Parallel loss of ndh genes in the core alismatid clade . 69 4.5 Discussion . 72 4.5.1 A refined phylogenetic backbone of Alismatales . 72 4.5.2 Rate heterogeneity and phylogenetic inference . 76 4.5.3 Loss of NADH dehydrogenase subunit genes . 79 4.5.4 Future work on the Alismatales backbone . 80 4.6 Conclusions . 81 vii 5 Dating early events in monocot phylogeny . 82 5.1 Summary . 82 5.2 Introduction . 83 5.3 Materials and methods . 85 5.3.1 Taxonomic and genomic assembly . 85 5.3.2 Phylogeny estimation . 86 5.3.3 Fossil constraints . 88 5.3.4 Molecular dating . 102 5.4 Results . 103 5.4.1 Phylogenetic inference . 103 5.4.2 Dating analysis . 110 5.5 Discussion . 111 5.5.1 Monocot phylogeny . 114 5.5.2 Dating analysis . 130 5.6 Conclusions . 134 6 Conclusion ..............................135 6.1 Overview . 135 6.2 Limitations of the methodology . 138 6.3 Future directions . 142 6.4 Some conclusions . 144 Bibliography ...............................146 Appendices A Voucher information for Chapter 2 . 193 B Trithuria classification for Chapter 2 . 196 C Supplementary material for Chapter 3 . 198 C.1 Dating seed-plant phylogeny . 198 C.2 Dating the species tree of Hydatellaceae . 202 C.3 Biogeographic analysis of Hydatellaceae . 202 C.4 Niche evolution in Hydatellaceae . 207 C.5 Accessions for seed-plant dating . 216 D Voucher information for Chapter 4 . 218 E Voucher information for Chapter 5 . 221 viii List of Tables 2.1 Phylogenetic ANOVAs of sexuality and quantitative characters 29 2.2 Summary of the new sectional treatment of Trithuria . 33 3.1 Ancestral climate variables for Hydatellaceae . 52 4.1 Comparison of the support values for interfamilial relationships 73 4.2 MP and ML support values for relationships among the petaloid families of Alismatales . 78 5.1 The PF16 partitioning scheme . 87 5.2 Monocot fossils used as molecular dating constraints . 89 5.3 Partition scheme comparisons . 104 5.4 Ages of major monocot clades . 127 C.1 Calibration fossils for seed-plant phylogeny . 200 C.2 Inferred ages of splits in seed-plant phylogeny . 201 C.3 Ages of nodes in Hydatellaceae . 204 C.4 Specimen accessions . 210 ix List of Figures 1.1 Summary of angiosperm relationships . 3 1.2 Summary of higher-order monocot relationships . 6 2.1 Maximum likelihood phylograms of Hydatellaceae . 23 2.2 Portion of the plastid tree including Trithuria occidentalis . 25 2.3 Bayesian multispecies coalescent estimate of species phylogeny 26 2.4 Reconstructions of ancestral character states . 27 2.5 Plots of characters associated with changes in sexuality . 31 3.1 Bayesian random-local-clock dating of seed-plant phylogeny . 45 3.2 Biogeography of Hydatellaceae . 47 4.1 Placement of Alismatales in monocot phylogeny . 64 4.2 A section of the ML tree Figure 4.1, focused on Alismatales .
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