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Generation Approach to Systematics in the Classic Reticulate Polypodium Vulgare Species Complex (Polypodiaceae)

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Generation Approach to Systematics in the Classic Reticulate Polypodium Vulgare Species Complex (Polypodiaceae) A Next-Generation Approach to Systematics in the Classic Reticulate Polypodium vulgare Species Complex (Polypodiaceae) by Erin Mackey Sigel Department of Biology Duke University Date:_______________________ Approved: ___________________________ Kathleen M. Pryer, Supervisor ___________________________ Paul S. Manos ___________________________ A. Jonathan Shaw ___________________________ John Willis ___________________________ Michael D. Windham Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2014 ABSTRACT A Next-Generation Approach to Systematics in the Classic Reticulate Polypodium vulgare Species Complex (Polypodiaceae) by Erin Mackey Sigel Department of Biology Duke University Date:_______________________ Approved: ___________________________ Kathleen M. Pryer, Supervisor ___________________________ Paul S. Manos ___________________________ A. Jonathan Shaw ___________________________ John Willis ___________________________ Michael D. Windham An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2014 Copyright by Erin Mackey Sigel 2014 ABSTRACT The Polypodium vulgare complex (Polypodiaceae) comprises a well-studied group of fern taxa whose members are cryptically differentiated morphologically and have generated a confusing and highly reticulate species cluster. Once considered a single species spanning much of northern Eurasia and North America, P. vulgare has been segregated into approximately 17 diploid and polyploid taxa as a result of cytotaxonomic work, hybridization experiments, and isozyme studies conducted during the 20th century. Despite considerable effort, however, the evolutionary relationships among the diploid members of the P. vulgare complex remain poorly resolved, and several taxa, particularly allopolyploids and their diploid progenitors, remain challenging to delineate morphologically due to a dearth of stable diagnostic characters. Furthermore, compared to many well-studied angiosperm reticulate complexes, relatively little is known about the number of independently-derived lineages, distribution, and evolutionary significance of the allopolyploid species that have formed recurrently. This dissertation is an attempt to advance systematic knowledge of the Polypodium vulgare complex and establish it as a “model” system for investigating the evolutionary consequences of allopolyploidy in ferns. Chapter I presents a diploids-only phylogeny of the P. vulgare complex and related species to test previous hypotheses concerning relationships within Polypodium iv sensu stricto. Analyses of sequence data from four plastid loci (atpA, rbcL, matK, and trnG-trnR) recovered a monophyletic P. vulgare complex comprising four well-supported clades. The P. vulgare complex is resolved as sister to the Neotropical P. plesiosorum group and these, in turn, are sister to the Asian endemic Pleurosoriopsis makinoi. Divergence time analyses incorporating previously derived age constraints and fossil data provide support for an early Miocene origin for the P. vulgare complex and a late Miocene-Pliocene origin for the four major diploid lineages of the complex, with the majority of extant diploid species diversifying from the late Miocene through the Pleistocene. Finally, node age estimates are used to reassess previous hypotheses, and to propose new hypotheses, about the historical events that shaped the diversity and current geographic distribution of the diploid species of the P. vulgare complex. Chapter II addresses reported discrepancies regarding the occurrence of Polypodium calirhiza in Mexico. The original paper describing this taxon cited collections from Mexico, but the species was omitted from the recent Pteridophytes of Mexico. Originally treated as a tetraploid cytotype of P. californicum, P. calirhiza now is hypothesized to have arisen through hybridization between P. glycyrrhiza and P. californicum. The allotetraploid can be difficult to distinguish from either of its putative parents, but especially so from P. californicum. These analyses show that a combination of spore length and abaxial rachis scale morphology consistently distinguishes P. calirhiza from P. californicum and confirm that both species occur in Mexico. Although v occasionally found growing together in the United States, the two species are strongly allopatric in Mexico, where P. californicum is restricted to coastal regions of the Baja California peninsula and neighboring Pacific islands and P. calirhiza grows at high elevations in central and southern Mexico. The occurrence of P. calirhiza in Oaxaca, Mexico, marks the southernmost extent of the P. vulgare complex in the Western Hemisphere. Chapter III examines a case of reciprocal allopolyploid origins in the fern Polypodium hesperium and presents it as a natural model system for investigating the evolutionary potential of duplicated genomes. In allopolyploids, reciprocal crosses between the same progenitor species can yield lineages with different uniparentally inherited plastid genomes. While likely common, there are few well-documented examples of such reciprocal origins. Using a combination of uniparentally inherited plastid and biparentally inherited nuclear sequence data, we investigated the distributions and relative ages of reciprocally formed lineages in Polypodium hesperium, an allotetraploid fern that is broadly distributed in western North America. The reciprocally-derived plastid haplotypes of Polypodium hesperium are allopatric, with populations north and south of 42˚ N latitude having different plastid genomes. Biogeographic information and previously estimated ages for the diversification of its diploid progenitors, lends support for middle to late Pleistocene origins of P. hesperium. Several features of Polypodium hesperium make it a particularly promising system for vi investigating the evolutionary consequences of allopolyploidy. These include reciprocally derived lineages with disjunct geographic distributions, recent time of origin, and extant diploid progenitor lineages. This dissertation concludes by demonstrating the utility of the allotetraploid Polypodium hesperium for understanding how ferns utilize the genetic diversity imparted by allopolyploidy and recurrent origins. Chapter IV details the use of high-throughput sequencing technologies to generate a reference transcriptome for Polypodium, a genus without preexisting genomic resources, and compare patterns of total and homoeolog- specific gene expression in leaf tissue of reciprocally formed lineages of P. hesperium. Genome-wide expression patterns of total gene expression and homoeolog expression ratios are strikingly similar between the lineages—total gene expression levels mirror those of the diploid progenitor P. amorphum and homoeologs derived from P. amorphum are preferentially expressed. The unprecedented levels of unbalanced expression level dominance and unbalanced homoeolog expression bias found in P. hesperium supports the hypothesis that these phenomena are pervasive consequences of allopolyploidy in plants. v ii For my parents, Mary and Milton, and my husband, Brian. viii TABLE OF CONTENTS Abstract…………………………………………..………………………………………………iv List of Tables………………………………………………………………………………..…….x List of Figures………………………………………………………………………………...…xii Acknowledgements…………………………………………………………………………....xiv Introduction………………………………………………………………………………………1 Chapter I: Phylogeny, divergence time estimates, and phylogeography of the diploid species of the Polypodium vulgare complex……………..……………………………………...8 Chapter II: Rediscovery of Polypodium calirhiza (Polypodiaceae) in Mexico………..…….49 Chapter III: Evidence for reciprocal origins in Polypodium hesperium (Polypodiaceae): a natural fern model system for investigating how multiple origins shape allopolyploid genomes……………………………….…………………….……………………………….......67 Chapter IV: Expression level dominance and homoeolog expression bias in reciprocal origins of the allopolyploid fern Polypodium hesperium……………………………..……...93 Chapter V: Additional insights into the evolution, diversification, and biogeography of ferns.……...……...…...………………………………………………………………………...133 Appendix A: Supplementary information for Chapter I………………………...……......136 Appendix B: Supplementary information for Chapter III…………..……………........….141 Appendix C: Supplementary information for Chapter IV…………..……………….....…144 References…………...……………………………………………………………………….....166 Biography…………...……………………………………………………………………….....189 ix LIST OF TABLES Table 1. Statistics for Chapter I plastid datasets and phylogenies..……………………......42 Table 2. Specimens of Polypodium used in Chapter II………………………………….........61 Table 3. Specimens of Polypodium and Pleurosoriopsis used in Chapter III………………..86 Table 4. Tree statistics for the plastid and nuclear sequence datasets analyzed in Chapter III…..……………………………………………………………………………………………...89 Table 5. Terms related to gene expression in allopolyploid organisms as described in Rapp et al. (2009) and Grover et al. (2012)………..…………………………………………124 Table 6. Synopsis of Polypodium specimens used in Chapter IV………………………….125 Table A.1. Voucher table of specimens included in Chapter I.…………………………...136 Table A. 2. Node age constraints obtained from Schuettpelz and Pryer (2009) for nodes in Fig. 5 of Chapter I…………………………………………………………………………..138 Table
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