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Phalaris, Poaceae) Evolutionary history of the canary grasses (Phalaris, Poaceae) Stephanie M. Voshell Dissertation submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy In Biological Sciences Khidir W. Hilu, Committee Chair Robert H. Jones Brent D. Opell John G. Jelesko May 1, 2014 Blacksburg, VA Keywords: Phalaris, polyploidy, phylogenetics, phylogeography, chromosome evolution Evolutionary history of the canary grasses (Phalaris, Poaceae) Stephanie M. Voshell ABSTRACT Canary grasses (Phalaris, Poaceae) include 21 species widely distributed throughout temperate and subtropical regions of the world with centers of diversity in the Mediterranean Basin and western North America. The genus contains annual/perennial, endemic/cosmopolitan, wild, and invasive species with basic numbers of x=6 (diploid) and x=7 (diploid/tetraploid/hexaploid). The latter display vastly greater speciation and geographic distribution. These attributes make Phalaris an ideal platform to study species diversification, dispersal, historic hybridization, polyploidy events, and chromosome evolution in the grasses. This body of research presents the first molecular phylogenetic and phylogeographic reconstruction of the genus based on the nuclear ITS and plastid trnT-F DNA regions allowing species relationships and the importance of polyploidy in speciation to be assessed. Divergence dates for the genus were determined using Bayesian methods (BEAST, version 1.6.2) and historic patterns of dispersal were analyzed with RASP (version 2.1b). Self-incompatibility and the feasibility of hybridization between major groups within the genus were studied with a series of greenhouse experiments. Acetocarmine and fluorescent staining techniques were used to study the morphology of the chromosomes in a phylogenetic context and the nuclear DNA content (C values) was quantified using flow cytometry. Four major clades were revealed in the genus with cytological and geographic affinities leading to the establishment of two subgenera and four sections in the first comprehensive infrageneric treatment of Phalaris. Divergence dating revealed a Miocene emergence (20.6-8.4 MYA) for the genus which is concurrent with studies of other genera in the Aveneae tribe. The hypothesis stating that Phalaris originated in the Mediterranean Basin and dispersed to the New World via a western route leading to a secondary center of diversification in western North America was supported by phylogeographic and cytological analyses. An empirical study comparing the weight, length, and width of the florets by morphological type and cytotype revealed significant differences that support a dispersal advantage among the New World and Arundinacea species. The x=6 species displayed greater intraspecific C value variation, higher DNA content per haploid chromosome set, and a distinct karyotype compared with the x=7 species indicating a complex history of chromosome evolution. iii ACKNOWLEDGEMENTS I am thankful to my advisor, Dr. Khidir Hilu for his support and encouragement throughout my graduate program. Dr. Hilu’s guidance with my research and professional development has been invaluable from start to finish. Dr. Opell, Dr. Jones, and Dr. Jelesko served on my advisory committee and I am thankful for their contributions to my project and the enlightening scientific discussions they provided during my committee meetings. I am thankful to Dr. Baldini, our colleague at the University of Florence, for his support and assistance with my research. I could not have asked for better colleagues during my time in the Hilu Lab. Sheena Friend, Sunny Crawley, Atia Eisa, and Alex Sumadijaya were incredibly supportive as fellow graduate students in the lab. It was a pleasure to work with my undergraduate researchers, Alyssa Hosey and Katy Lawler, who provided invaluable assistance with many aspects of my research. The members of the Biological Sciences Department helped make my experience in graduate school so wonderful and I can’t thank everyone enough for that! All the encouragement and support I received while pursuing my interests in both research and teaching will never be forgotten. Lastly, I thank my friends and family for their guidance, support, and understanding while I pursued my degree. You all mean the world to me! iv DEDICATION To my parents, for inspiring my interest in nature and science. v TABLE OF CONTENTS Abstract………………………………………………………………………………ii Acknowledgements…………………………………………………………………..iv Dedication……………………………………………………………………………v Table of Contents………………………………………………………………….....vi List of Tables………………………………………………………………………...viii List of Figures………………………………………………………………………..ix Attribution……………………………………………………………………………xi Introduction (Literature Review)……………………………………………….…1 Literature Cited………………………………………………………………………6 Chapter 1. Canary grasses (Phalaris, Poaceae): Molecular phylogenetics, polyploidy and floret evolution……………………………………12 Abstract………………………………………………………………………………12 Introduction…………………………………………………………………………..13 Materials and Methods……………………………………………………………….17 Results………………………………………………………………………………..21 Discussion…………………………………………………………………………....30 Acknowledgements…………………………………………………………………..38 Literature Cited………………………………………………………………………39 Chapter 2. Canary Grasses (Phalaris, Poaceae): Biogeography, molecular dating and the role of floret structure in dispersal………………...…49 Abstract………………………………………………………………………………49 Introduction…………………………………………………………………………..50 Materials and Methods……………………………………………………………….57 Results………………………………………………………………………………..61 Discussion……………………………………………………………………………67 Acknowledgements…………………………………………………………………..77 Literature Cited………………………………………………………………………77 Chapter 3. Canary grasses (Phalaris, Poaceae): Infrageneric treatment based on molecular phylogenetics and floret structure………………89 Abstract………………………………………………………………………………89 Introduction…………………………………………………………………………..89 Materials and Methods……………………………………………………………….94 Results………………………………………………………………………………..96 vi Discussion……………………………………………………………………………101 Proposed Infrageneric Classification………………………………………...………103 Key to Subgenera and Sections……………………………………………………...118 Literature Cited……………………………………………………………………....119 Chapter 4. Canary grasses (Phalaris, Poaceae): breeding systems, floret morphology and genome size……………………………………………….126 Abstract……………………………………………………………………………...126 Introduction………………………………………………………………………….127 Materials and Methods………………………………………………………………130 Results…………………………………………………………………………….....134 Discussion…………………………………………………………………………...150 Acknowledgements……………………………………………………………….....157 Literature Cited………………………………………………………………….......157 Chapter 5. Canary grasses (Phalaris, Poaceae): cytology, genome size and origins of aneuploidy…………………………………………………….166 Abstract……………………………………………………………………………..166 Introduction………………………………………………………………………....167 Materials and Methods……………………………………………………………...171 Results……………………………………………………………………………....174 Discussion…………………………………………………………………………..178 Acknowledgements………………………………………………………………....185 Literature Cited……………………………………………………………………..186 vii LIST OF TABLES Table 2.1. Phalaris species used, chromosome number (2n = somatic chromosome number), floret type, and geographic region(s) of distribution…………………74 Table 3.1. Currently recognized Phalaris species and respective information regarding chromosome number and polyploid level, geographic range, habit, and floret type……………………………………………………………………………...91 Table 4.1. 2C values calculated from flow cytometry………………………………...144 Table 4.2. Percent of bagged and unbagged (control) Phalaris inflorescences Producing caryopses………..………………………………………………….146 Table 4.3. Percent of spikelets producing caryopses for bagged and unbagged inflorescences in Phalaris………………………………………………….......147 Table 4.4. Attempted crosses to generate Phalaris hybrids and success rate of germination…………………………………………………………………….149 Appendix A. Phalaris species used, geographic origin of the material, information on the herbarium vouchers, and GenBank numbers are noted…………………….47 Appendix B. Taxa used, their geographic origin, herbarium voucher information, and GenBank numbers……………………………………………………….…..…125 Appendix C. Summary of floret morphology data. Means, standard deviation, and standard error are presented for floret weight, length and width by floret type, cytotype and species …………………………………………………..…........162 viii LIST OF FIGURES Fig. 1.1 Geographic distribution of canary grasses (Phalaris)………………………….13 Fig. 1.2. A diagrammatic illustration of six floret types recognizable in species of Phalaris following Anderson (1961) and Baldini (1995)………………………..14 Fig. 1.3. ITS phylogram based on Bayesian inference………………………………......24 Fig. 1.4. trnT-F phylogram generated from Bayesian inference………………………...27 Fig. 1.5. Combined ITS and trnT-F phylogeny based on maximum parsimony and Bayesian inference……………………………………………………………….29 Fig. 2.1 Global distribution of Phalaris species……………………………………...…51 Fig. 2.2 Estimated dates of divergence within Phalaris based on the ITS dataset using BEAST v1.6.2.…………………………………………………………………..53 Fig. 2.3 Ancestral node reconstruction and dispersal-vicariance analysis generated in RASP from the ITS data set……………………………………………………..64 Fig. 2.4 Ancestral node reconstruction and dispersal-vicariance analysis generated in RASP from the trnT-F data set…………………………………………………..66 Fig. 2.5 Estimated dates of divergence within Phalaris based on the trnT-F dataset using
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