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Snow White and Rose Red: Studies on the Contrasting Evolutionary Trajectories of the Genera Leucanthemum Mill

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Snow White and Rose Red: Studies on the Contrasting Evolutionary Trajectories of the Genera Leucanthemum Mill Snow White and Rose Red: Studies on the contrasting evolutionary trajectories of the genera Leucanthemum Mill. and Rhodanthemum B.H.Wilcox & al. (Compositae, Anthemideae) DISSERTATION ZUR ERLANGUNG DES DOKTORGRADES DER NATURWISSENSCHAFTEN (DR. RER. NAT.) DER FAKULTÄT FÜR BIOLOGIE UND VORKLINISCHE MEDIZIN DER UNIVERSITÄT REGENSBURG vorgelegt von Florian Wagner aus Burgstall (Mitwitz) Juli 2019 Das Promotionsgesuch wurde eingereicht am: 12.07.2019 Die Arbeit wurde angeleitet von: Prof. Dr. Christoph Oberprieler Unterschrift: ……………………………....... Florian Wagner iv Abstract Plant systematics, the study of taxonomy, phylogeny and evolutionary processes in plants has undergone considerable progress in the last decades. The application of modern molecular approaches and DNA-sequencing techniques in the field has led to an improved inventory of biodiversity and a better understanding of evolutionary processes shaping the biological diversity on our planet. The increased availability of molecular and genomic data has particularly facilitated the investigation of shallowly diverged and taxonomically complex taxon-groups, which is challenging due to minor morphological differences, low genetic differentiation and/or hybridization among taxa. The present thesis investigates species delimitation, hybridization and polyploidization in the recently diverged genera Leucanthemum Mill. and Rhodanthemum B.H. Wilcox & al. of the subtribe Leucantheminae K.Bremer & Humphries (Compositae, Anthemideae) by applying Sanger-, 454-pyro-, and restriction site associated DNA (RAD) sequencing, as well as AFLP-fingerprinting and morphometric analyses. The first two parts are focusing on species delimitation and hybridization in the closely-knit taxon groups around L. ageratifolium Pau and R. arundanum B.H. Wilcox & al., respectively. Various analyses based on AFLP fingerprinting, RADseq and multi-locus sequence data demonstrate that the robustness of species delimitation results is considerably influenced by the intensity of hybridization among species and the number of hybrid individuals included. Therefore, a step-by-step approach is performed in both studies, with an initially step of identification and subsequent removal of hybrid individuals, followed by application of different species-delimitation methods. This strategy results in the reliable identification of independent species, subspecies and nothospecies in both taxonomically complex plant groups. The third part of the present thesis compares the contrasting evolutionary trajectories of diploid representatives of both genera in a more comprehensive phylogenetic study. Specific hypotheses for the formation of polyploids in plants are proposed and evaluated to find factors that promote polyploidization in certain plant groups (e.g., Leucanthemum) and not in others (e.g., Rhodanthemum). Multi-locus sequence data from 127 accessions of the subtribe Leucantheminae unveil a significantly higher genetic divergence and hybridization signal among diploid lineages of Leucanthemum compared to Rhodanthemum, in spite of a similar crown age and diversification pattern during the Quaternary. The study demonstrates the importance of genetic differentiation among diploid progenitors and their concurrent affinity for natural hybridization for the formation of a polyploid complex. Furthermore, the role of climate-induced range overlaps on hybridization and polyploid speciation during the Quaternary is discussed. v References of published and submitted manuscripts The underlying thesis is composed of the following published or submitted manuscripts. The proposed nomenclatural changes/novelties are not intended being effectively published in the present thesis. A. Wagner F, Härtl S, Vogt R, Oberprieler C. 2017. 'Fix Me Another Marguerite!': Species delimitation in a group of intensively hybridizing lineages of ox-eye daisies (Leucanthemum Mill., Compositae-Anthemideae). Molecular Ecology 26: 4260– 4283. B. Wagner F, Ott T, Schall M, Lautenschlager U, Vogt R, Oberprieler C. Taming the Red Bastards: Hybridization and species delimitation in the Rhodanthemum arundanum-group (Compositae-Anthemideae). Molecular Phylogenetics and Evolution doi: 10.1016/ympev.2019.106702. C. Wagner F, Ott T, Zimmer C, Reichhart V, Vogt R, Oberprieler C. 2019. 'At the crossroads towards polyploidy': Genomic divergence and extent of homoploid hybridization are drivers for the formation of the ox-eye daisy polyploid complex (Leucanthemum Mill., Compositae-Anthemideae). New Phytologist 223: 2039– 2053. In the course of my PhD, I contributed to further publications, which are not part of the thesis: D. Konowalik K, Wagner F, Tomasello S, Vogt R, Oberprieler C. 2015. Detecting reticulate relationships among diploid Leucanthemum Mill. (Compositae, Anthemideae) taxa using multilocus species tree reconstruction methods and AFLP fingerprinting. Molecular Phylogenetics and Evolution 92: 308–328. E. Oberprieler C, Wagner F, Tomasello S, Konowalik K. 2017. A permutation approach for inferring species networks from gene trees in polyploid complexes by minimizing deep coalescences. Methods in Ecology and Evolution 8: 835–849. F. Hassanpour H, Zare-Maivan H, Sonboli A, Kazempor-Osaloo S, Wagner F, Tomasello S, Oberprieler C. 2018. Phylogenetic species delimitation unravels a new species in the genus Sclerorhachis (Rech.f.) Rech.f. (Compositae, Anthemideae). Plant Systematics and Evolution 304: 185–203. vi G. Oberprieler C, Hassanpour H, Sonboli A, Ott T, Wagner F. 2019. Multi-locus phylogenetic reconstructions reveal ample reticulate relationships among genera in Anthemideae subtribe Handeliinae (Compositae). Plant Systematics and Evolution doi: 10.1007/s00606-019-01588-0. H. Oberprieler C, Schinhärl L, Wagner F, Hugot L, Vogt R. Karyological and molecular-genetic analyses of Leucanthemum Mill. (Compositae, Anthemideae) in Corsica. Submitted for publication to Willdenowia (under review). Personal contributions Publication A Florian Wagner (FW), Robert Vogt (RV), and Christoph Oberprieler (CO) conceived this study. FW and Sabine Härtl (SH) produced the sequence and AFLP fingerprint data, which were analyzed by FW. FW wrote a first draft of the study, which was complemented and partly rewritten by RV and CO. Publication B FW, RV, and CO conceived the present study and collected plant material. Maximilian Schall (MS) produced the Sanger sequence data, which were processed and analyzed together with the RADseq data by Tankred Ott (TO), FW, and Ulrich Lautenschlager (UL). A first draft of the paper was written by FW with input from RV and CO. Publication C FW, RV, and CO conceived the present study. FW, Claudia Zimmer (CZ) and Verena Reichhart (VR) produced the sequence data, which was processed by TO and FW and analysed by FW. A first draft of the paper was written by FW with input from RV and CO. vii Contents Abstract .................................................................................................................................. v References of published and submitted manuscripts .............................................................vi Personal contributions ........................................................................................................... vii Chapter 1: General introduction ........................................................................................ 1 1.1 Plant systematics in the era of next-generation sequencing ......................................... 1 1.2 Species delimitation in the framework of the multi-species coalescent ....................... 2 1.3 What we still don’t know about polyploidy ................................................................. 2 1.4 The subtribe Leucantheminae ...................................................................................... 3 1.5 Thesis outline ............................................................................................................... 4 Chapter 2: Fix Me Another Marguerite! ........................................................................... 9 Abstract .............................................................................................................................. 9 2.1 Introduction ................................................................................................................ 10 2.2 Materials and Methods ............................................................................................... 12 2.2.1 Plant material and DNA extraction ..................................................................... 12 2.2.2 AFLP fingerprinting ............................................................................................ 13 2.2.3 Detection of potential hybrid individuals ............................................................ 17 2.2.4 Plastid and nuclear marker sequencing ............................................................... 18 2.2.5 Multiple sequence alignments and gene-tree reconstructions ............................. 18 2.2.6 MSC species-delimitation ................................................................................... 19 2.3 Results ........................................................................................................................ 21 2.3.1 AFLP fingerprinting ............................................................................................ 21 2.3.2 Detection of potential hybrid individuals ............................................................ 22 2.3.3 Multiple sequence alignments and gene-tree
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