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Scrophulariaceae) and Hemiparasitic Orobanchaceae (Tribe Rhinantheae) with Emphasis on Reticulate Evolution

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Scrophulariaceae) and Hemiparasitic Orobanchaceae (Tribe Rhinantheae) with Emphasis on Reticulate Evolution Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie der Ludwig-Maximilians-Universität München Evolutionary history and biogeography of the genus Scrophularia (Scrophulariaceae) and hemiparasitic Orobanchaceae (tribe Rhinantheae) with emphasis on reticulate evolution vorgelegt von Agnes Scheunert München, Dezember 2016 II Diese Dissertation wurde angefertigt unter der Leitung von Prof. Dr. Günther Heubl an der Fakultät für Biologie, Department I, Institut für Systematische Botanik und Mykologie an der Ludwig-Maximilians-Universität München Erstgutachter: Prof. Dr. Günther Heubl Zweitgutachter: Prof. Dr. Jochen Heinrichs Tag der Abgabe: 15.12.2016 Tag der mündlichen Prüfung: 22.03.2017 III IV Eidesstattliche Versicherung und Erklärung Eidesstattliche Versicherung Ich, Agnes Scheunert, versichere hiermit an Eides statt, daß die vorgelegte Dissertation von mir selbständig und ohne unerlaubte Hilfe angefertigt ist. München, den 14.12.2016 ______________________________________ Agnes Scheunert Erklärung Diese Dissertation wurde im Sinne von § 12 der Promotionsordnung von Prof. Dr. Günther Heubl betreut. Hiermit erkläre ich, Agnes Scheunert, dass die Dissertation nicht ganz oder in wesentlichen Teilen einer anderen Prüfungskommission vorgelegt worden ist, und daß ich mich anderweitig einer Doktorprüfung ohne Erfolg nicht unterzogen habe. München, den 14.12.2016 ______________________________________ Agnes Scheunert V VI Declaration of author contribution In this cumulative thesis, I present the results of my doctoral research, which was conducted at the Ludwig-Maximilians-Universität of Munich under the supervision of Prof. Dr. Günther Heubl. The results of my research have been published or accepted for publication in international peer-reviewed journals. The four articles included in this dissertation are presented in chapter 4; all of them have resulted from collaboration with other scientists, and my contributions to each of them were as follows: Article I: Scheunert A, Fleischmann A, Olano-Marín C, Bräuchler C, Heubl G. 2012. Phylogeny of tribe Rhinantheae (Orobanchaceae) with a focus on biogeography, cytology and re- examination of generic concepts. Taxon 61(6): 1269-1285. The study was designed by G. Heubl and C. Bräuchler. I did the conceptual design of the methodical treatment of incongruence, and conducted most of the respective analyses. I revised the manuscript, coordinated generation of complementary sequences and did their editing and alignment, re-analyzed most of the data, did the final phylogenetic analyses and interpreted the results. I wrote large parts of the Material and Methods and Results sections and created most of the figures. A. Fleischmann co-supervised the study, selected the taxon sampling, determined the plant material and interpreted the results. He helped to draft the manuscript, wrote large parts of the Introduction and Discussion including the taxonomic treatment, made the taxonomic combinations, and contributed photographs to the manuscript. C. Olano-Marín conducted the laboratory work, did most of the initial phylogenetic analyses, provided a photograph and contributed to the manuscript. C. Bräuchler helped with the selection of herbarium material, improved the manuscript in its initial phase, created some of the graphics and submitted the sequence data to NCBI's Genbank. G. Heubl supervised the work, helped with the conception of the manuscript and improved and corrected the manuscript. Article II: Scheunert A, Heubl G. 2011. Phylogenetic relationships among New World Scrophularia L. (Scrophulariaceae): new insights inferred from DNA sequence data. Plant Systematics and Evolution 291: 69-89. G. Heubl designed the study. I selected the taxon sampling, and did the laboratory work including DNA extraction, PCR amplification and product purification, sequencing, and subsequent sequence editing, alignment and phylogenetic analyses. I also planned and performed the dating analyses and the statistical tests. I interpreted the results, wrote the manuscript and created the figures, tables and maps. G. Heubl supervised the study, the laboratory work and the phylogenetic analyses, helped to interpret the data and improved the manuscript. VII Article III: Scheunert A, Heubl G. 2014. Diversification of Scrophularia (Scrophulariaceae) in the Western Mediterranean and Macaronesia - phylogenetic relationships, reticulate evolution and biogeographic patterns. Molecular Phylogenetics and Evolution 70: 296- 313. The study was designed by G. Heubl and myself. I selected the taxon sampling, cultivated several of the plants in the greenhouses of the Botanical Garden in Munich, and determined the used specimens. I designed the methodical concept to address hybridization and incongruence, including the use of phylogenetic networks and the taxon duplication approach in combination with ancestral area reconstruction. I supervised the laboratory work, did editing and alignment of sequence data, conducted the statistical tests, performed the phylogenetic analyses, indel coding and biogeographic reconstruction, and created the haplotype and consensus networks. Finally I interpreted the results, wrote the manuscript and prepared the figures, tables and maps. G. Heubl supervised the study, helped to interpret the results and improved and corrected the manuscript. Article IV: Scheunert A, Heubl G. Against all odds: reconstructing the evolutionary history of Scrophularia (Scrophulariaceae) despite high levels of incongruence and reticulate evolution. Organisms Diversity and Evolution, in press. doi: 10.1007/s13127-016-0316-0 G. Heubl and myself developed the concept of the study. I generated sequence data and supervised the laboratory work. I conducted an extensive literature search on the topics of among-dataset incongruence, possible treatments of intra-individual-polymorphism, and the evolutionary characteristics of ITS. Based on this I compiled the workflow used in the study to examine hybridization and other sources of phylogenetic incongruence and ambiguity. I conducted indel and character coding and compared the available methods. I performed data analysis (statistical tests, phylogenetic tree reconstruction, biogeography, divergence dating, consensus and Neighbor-Net networks) and interpretation, wrote the manuscript and prepared the figures, tables and the dispersal map. G. Heubl supervised the study and improved and shortened the manuscript. Munich, 13/12/2016 ____________________________________________ Agnes Scheunert ____________________________________________ Prof. Dr. Günther Heubl (supervisor) All photographs, images and illustrations in this work were made by Agnes Scheunert unless denoted otherwise. VIII Funding My doctoral studies were financially supported for two years (November 2007 - October 2009) by a scholarship, provided by the "Universität Bayern e.V.". Graduate funding was granted based on the "Bayerisches Eliteförderungsgesetz" (BayEFG) and included a salary and facultatively also travel expenses. IX X Für meine Mama. XI XII Contents Preface Eidesstattliche Versicherung und Erklärung V Declaration of author contribution VII Funding IX Dedication XI Contents XIII 1. Summary / Zusammenfassung 1 2. Introduction 5 2.1. Biology and Systematics of Scrophulariaceae Juss. 5 2.1.1. Traditional circumscription of Scrophulariaceae 5 2.1.2. Current understanding of phylogenetic relationships 6 2.2. Parasitism in plants: the example of Orobanchaceae Vent. 10 2.2.1. Parasitism 10 2.2.2. Orobanchaceae Vent. 10 2.2.3. Tribe Rhinantheae Lam. & DC. 12 2.3. The genus Scrophularia L. 13 2.3.1. Taxonomic history 13 2.3.2. Morphology, distribution and phylogenetic relationships 14 2.3.3. Pollination biology and evolution of the staminode 18 2.3.4. Anatomy and phytochemistry 19 3. Methodology 21 3.1. Testing for incongruence among phylogenetic trees 21 3.2. Combining incongruent datasets for phylogenetic tree construction 22 3.3. Character and indel coding 22 3.4. Network methods 25 4. Scientific manuscripts 29 4.1. Article I: Phylogeny of tribe Rhinantheae (Orobanchaceae) with a focus on biogeography, cytology and re-examination of generic concepts 31 4.2. Article II: Phylogenetic relationships among New World Scrophularia L. (Scrophulariaceae): new insights inferred from DNA sequence data 51 XIII 4.3. Article III: Diversification of Scrophularia (Scrophulariaceae) in the Western Mediterranean and Macaronesia - Phylogenetic relationships, reticulate evolution and biogeographic patterns 75 4.4. Article IV: Against all odds: reconstructing the evolutionary history of Scrophularia (Scrophulariaceae) despite high levels of incongruence and reticulate evolution 95 5. General Discussion 125 5.1. Phylogenetic relationships in Rhinantheae and taxonomic implications 125 5.2. The biogeographic history of Scrophularia 128 5.2.1. Eastward migrations 130 5.2.2. Westward migrations 130 5.3. The influence of geography and topography on diversification 132 5.3.1. Origin and expansion of Scrophularia 132 5.3.2. Diversification in the Irano-Turanian region and the Mediterranean 133 5.3.3. Diversification in Eastern Asia and the New World 134 5.4. The influence of hybridization on diversification 135 5.4.1. Phylogenetic tree incongruence and intra-individual polymorphism 135 5.4.2. Hybrid speciation in Scrophularia - homoploid hybrid species 137 5.4.3. Allopolyploid hybrid species and hybrid lineages 139 5.4.4. Combined effects of topography, hybridization and climate
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