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Phylogenetics and Molecular Evolution of Alismatales Based on Whole Plastid Genomes

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Phylogenetics and Molecular Evolution of Alismatales Based on Whole Plastid Genomes PHYLOGENETICS AND MOLECULAR EVOLUTION OF ALISMATALES BASED ON WHOLE PLASTID GENOMES by Thomas Gregory Ross B.Sc. The University of British Columbia, 2011 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIRMENTS FOR THE DEGREE OF MASTER OF SCIENCE in The Faculty of Graduate and Postdoctoral Studies (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) November 2014 © Thomas Gregory Ross, 2014 ABSTRACT The order Alismatales is a mostly aquatic group of monocots that displays substantial morphological and life history diversity, including the seagrasses, the only land plants that have re-colonized marine environments. Past phylogenetic studies of the order have either considered a single gene with dense taxonomic sampling, or several genes with thinner sampling. Despite substantial progress based on these studies, multiple phylogenetic uncertainties still remain concerning higher-order phylogenetic relationships. To address these issues, I completed a near- genus level sampling of the core alismatid families and the phylogenetically isolated family Tofieldiaceae, adding these new data to published sequences of Araceae and other monocots, eudicots and ANITA-grade angiosperms. I recovered whole plastid genomes (plastid gene sets representing up to 83 genes per taxa) and analyzed them using maximum likelihood and parsimony approaches. I recovered a well supported phylogenetic backbone for most of the order, with all families supported as monophyletic, and with strong support for most inter- and intrafamilial relationships. A major exception is the relative arrangement of Araceae, core alismatids and Tofieldiaceae; although most analyses recovered Tofieldiaceae as the sister-group of the rest of the order, this result was not well supported. Different partitioning schemes used in the likelihood analyses had little effect on patterns of clade support across the order, and the parsimony and likelihood results were generally highly congruent. I also used the inferred phylogeny of Alismatales to study the loss of the mostly plastid-encoded NADH dehydrogenase enzyme complex in the order. This enzyme is hypothesized to be involved in mitigating photooxidative stress by inducing chlororespiration. The inclusion or exclusion of ndh ii pseudogenes had little impact on the main phylogenetic results. Previous work hypothesized three independent losses/pseudogenization events within the core alismatids, which I confirmed here. I also inferred an additional loss in Tofieldiaceae, the first example in unsubmerged species of Alismatales. The repeated loss of plastid NADH dehydrogenase may spur future research into the physiological bases of the loss. iii PREFACE All steps of this work, including sequencing and analysis was conducted predominantly by me, but with the assistance of others at the following specific locations. Jerrold Davis (Cornell University) and Craig Barrett (California State Los Angeles) were responsible for sequencing 11 of the samples I used in my analysis: Sagittaria latifolia (Alismataceae), Amphibolis griffithii (Cymodoceaceae), Ruppia polycarpa (Cymodoceaceae), Najas guadalupensis (Hydrocharitaceae), Vallisneria americana (Hydrocharitaceae), Triglochin procera (Juncaginaceae), Posidonia ostenfieldii (Posidoniaceae), Potamogeton pectinatus (Potamogetonaceae), Zanichellia palustris (Potamogetonaceae), Scheuchzeria palustris (Scheuchzeriaceae), Zostera mulleri (Zosteraceae). Vivienne Lam (UBC) was responsible for sequencing, assembly and gene annotation of Lophiola aurea (Nartheciaceae) and Campynema lineare (Campynemataceae), and Marybel Soto Gomez (UBC) was responsible for sequencing, assembly and gene annotation of Burmannia bicolor (Burmanniaceae), Cyclanthus bipartitus (Cyclanthaceae), Freycinetia banksii (Pandanaceae), Stichoneuron caudatum (Stemonaceae) and Xerophyta retinervis (Velloziaceae). Additional thanks are due to Donald Les (University of Connecticut), Dennis Stevenson (New York Botanical Garden), John Conran (University of Adelaide), and Gitte Petersen (University of Copenhagen) who provided multiple plant samples as DNA or silica dried specimens. Bioinformatics scripting assistance was provided by David Tack (UBC) and Daisie Huang (UBC). iv TABLE OF CONTENTS ABSTRACT .................................................................................................................................... ii PREFACE ...................................................................................................................................... iv TABLE OF CONTENTS ................................................................................................................ v LIST OF TABLES ........................................................................................................................ vii LIST OF FIGURES ..................................................................................................................... viii ACKNOWLEDGMENTS ............................................................................................................. ix 1. INTRODUCTION ...................................................................................................................... 1 2. MATERIALS AND METHODS ................................................................................................ 4 2.1 Taxonomic sampling ............................................................................................................. 4 2.2 DNA and library preparation................................................................................................. 4 2.3 Contig assembly and plastid gene annotation ....................................................................... 6 2.4 Alignment and matrix construction ....................................................................................... 7 2.5 Error checking ....................................................................................................................... 8 2.6 Phylogenetic inference .......................................................................................................... 8 3. RESULTS ................................................................................................................................. 12 3.2 Relationships in core Alismatales ....................................................................................... 12 3.3 Loss of ndh genes ................................................................................................................ 13 4. DISCUSSION ........................................................................................................................... 14 4.1 The phylogenetic positions of Alismatales and Acorus in monocot phylogeny ................. 14 4.2 Resolving the first split in Alismatales phylogeny.............................................................. 15 4.3 Relationships in core alismatids: Higher-order relationships ............................................. 16 4.4 Relationships in core alismatids: The petaloid clade .......................................................... 17 4.5 Relationships in core alismatids: The tepaloid clade .......................................................... 19 4.6 Repeated loss of the plastid NADH dehydrogenase complex in Alismatales ..................... 22 4.7 Conclusion ........................................................................................................................... 25 FIGURES AND TABLES ............................................................................................................ 27 BIBLIOGRAPHY ......................................................................................................................... 38 v APPENDICES .............................................................................................................................. 47 vi LIST OF TABLES Table 1 Summary of bootstrap support for clades found in shortest trees for core alismatids that have less than 100% bootstrap in at least one parsimony or likelihood analysis ..................................................................................................................................28 Table 2 Species in Alismatales with pseudogenization or loss of at least one plastid-encoded ndh subunit gene ......................................................................................................29 Table S1 Specimen source information ..................................................................................47 Table S2 DNA substitutions models and partitioning scheme and partition subsets resulting from two different partition analyses conducted in PartitionFinder using the BIC criterion ....................................................................................................................51 vii LIST OF FIGURES Figure 1 Relationships among Araceae, core alismatids, and Tofieldiaceae inferred in parsimony and likelihood analyses ..........................................................................30 Figure 2 Core alismatid phylogeny inferred in a likelihood analysis of 83 plastid genes using the “GxC-n” partitioning scheme ............................................................................32 Figure 3 Parsimony reconstructions showing predicted losses of the NADH dehydrogenase complex genes in Alismatales .................................................................................34 Figure 4 Branch support in core alismatids compared to other studies .................................36
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