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Evolution of Mountain Plants in the Region of the Qinghai-Tibetan Plateau and Beyond

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Evolution of Mountain Plants in the Region of the Qinghai-Tibetan Plateau and Beyond Evolution of mountain plants in the region of the Qinghai-Tibetan Plateau and beyond Dissertation for attaining the PhD degree of Natural Sciences submitted to the faculty of Biological Sciences of the Goethe University Frankfurt in Frankfurt am Main by Sabine Matuszak from Leverkusen, Germany Frankfurt 2015 (D 30) 1 accepted by the faculty of Biological Sciences of the Goethe University Frankfurt as a dissertation. Dean: Prof. Dr. Meike Piepenbring First reviewer: Prof. Dr. Alexandra Muellner-Riehl Second reviewer: Prof. Dr. Georg Zizka Date of disputation: 2 SUMMARY Biodiversity is unevenly distributed on Earth. Highly diverse biotas are particularly expected in mountain systems, because altitudinal zonation provides a number of habitat alternatives, which could lead to lower extinction rates during climatic changes. Nevertheless, the impact of environmental changes on plant diversification (especially for sub-alpine taxa) in the course of mountain orogenesis remains poorly understood. This is also true for the highest and largest plateau on Earth, the Qinghai-Tibetan Plateau (QTP) and its surrounding areas. The predominant biome of the QTP is alpine tundra characterised by low precipitation, but especially the regions at the southern and southeastern flanks of the QTP harbour high levels of biodiversity due to more favourable climatic conditions. In total, there are four biodiversity hotspots surrounding the QTP: the Himalayas, the mountains of Central Asia, Indo-Burma, and the Hengduanshan. These hotspots are assumed to have resulted from geological and climatic changes caused by the uplift of the QTP. In this doctoral thesis, I investigated the impact of these environmental changes on plant diversification and the floristic exchange between the QTP region and biodiversity hotspots of Southeast Asia as well as other parts of the world by using the sub-alpine genera Agapetes and Vaccinium (Vaccinieae, Ericaceae) as well as Tripterospermum (Gentianinae, Gentianaceae) as model systems. Furthermore, I examined the role of niche evolution and conservatism in a changing environment over time, and detected possible beneficial morphological traits of plants in the surroundings of the QTP by investigating subtropical Gentianinae (Crawfurdia, Kuepferia, Metagentiana, Sinogentiana, and Tripterospermum; Gentianaceae). For Vaccinieae, a North American origin was found from where the tribe dispersed nearly throughout the world. In this case, the QTP region acted as a sink area, because this region was colonised several times from different parts of the world and diversification followed the ancestors’ arrival. The diversification of Vaccinieae started around 21.3 to 9.2 Ma in the QTP’s region, which temporally coincides with the early formation of the Himalayas and the 3 intensification of the monsoon system, suggesting a potential causal relationship. In contrast, Tripterospermum originated at the southeastern fringe of the QTP at about 8.8 to 2.7 Ma, and after in situ diversification other regions of Asia and Southeast Asia were colonised. Therefore, the QTP acted as a source area. Such a source pattern was often found for alpine taxa, but to be able to assess a general trend for sub-alpine groups, additional genera must be investigated in future research. Nevertheless, it could be possible that the impact of the QTP’s environmental changes might vary over time. During its early formation history the QTP could have acted as sink (Vaccinieae) and during more recent times as source area (Tripterospermum). The capsule- producing QTP genera Kuepferia and Sinogentiana (displaying a tendency towards niche conservatism) as well as Crawfurdia and Metagentiana (characterised by niche evolution) have fewer species and a smaller distribution range than Tripterospermum with berry-like fruits and a strong tendency towards niche evolution. Among other tested morphological traits, only the evolution of berry-like fruits has led to increased speciation rates and could therefore be viewed as potential key innovation. In the case of Tripterospermum it is likely that diversification was mediated by its wide niche breadth and good dispersal ability rather than environmental changes in the QTP region. This example stresses the importance to also consider the ecology of plant taxa when investigating possible correlations between environmental changes and diversification, which has only rarely been done so far for plants in the QTP region. 4 DECLARATION I confirm that the work presented in this thesis is my own with the following acknowledgments. Determination of Gentianaceae collected in a field trip to China in 2011 and re- determination of herbarium vouchers of Gentianaceae were done by Adrien Favre (chapters 2 and 3). For the published manuscript “Two new species of the Asian genus Tripterospermum (Gentianaceae)” by Adrien Favre, Sabine Matuszak, and Alexandra Muellner-Riehl, published in Systematic Botany in 2013, I was involved in finding one of the two described plants (Tripterospermum maculatum) and in measuring as well as critically evaluating morphological traits of the two species. Furthermore, I helped to conduct comparative statistical analyses (multivariate analyses). For the published manuscript “Two new genera of Gentianinae (Gentianaceae): Sinogentiana and Kuepferia supported by molecular phylogenetic evidence” by Adrien Favre, Sabine Matuszak, Hang Sun, Ende Liu, Yong-Ming Yuan, and Alexandra Muellner-Riehl, published in Taxon in 2014, I was involved in the lab work (PCR amplification and sequencing of the nuclear marker ITS and the plastid trnL-trnF region), as well as in phylogenetic analyses (chapter 5). The use of any other material from other sources and the scientific contributions from collaborators are fully acknowledged throughout the thesis. Sabine Matuszak Frankfurt am Main, 20th October 2015 5 ACKNOWLEDGEMENTS I would like to express my deep gratitude to my research supervisors Prof. Dr. Alexandra N. Muellner-Riehl and Dr. Adrien Favre for their support, patient guidance, valuable critique of this research work, and for giving me the opportunity to carry out this research on Agapetes, Vaccinium and Tripterospermum in the course of their funded projects. Especially the constant enthusiastic encouragement of Adrien Favre helped me through the final stages of this doctoral thesis. I would also like to thank Prof. Dr. Georg Zizka for acting as the second reviewer of my thesis and his support during the final stage of my thesis. I also wish to thank all collaboration partners for collecting and providing plant material, helping Adrien Favre and me in the course of our field trip to China in 2011, great scientific discussions, and constructive comments on the manuscripts: Prof. Dr. Hang Sun, Dr. Ende Liu, Dr. Chih-Hsiung Chen, and Dr. Jan Schnitzler. I would like to thank the very helpful and friendly staff of all the herbaria which provided plant material for my research: Frankfurt/Main (FR), Kunming (KUN), Leiden (L), Leipzig (LZ), Paris (P), Taichung (TNM), and Vienna (WU). I would also like to extend my thanks to the biological-technical assistants Heike Kappes, Frank Lappe, Maike Fibian, and Claudia Krueger for their valuable advice and support in the laboratory. Furthermore, I wish to acknowledge the help with analyses and methodological trouble-shooting provided by Jan Schnitzler, Ingo Michalak, Lars Nauheimer, Melanie Grudinski, Adrien Favre, and Daniele Silvestro. Many thanks also to Adrien Favre, Astrid Jakob and Alexandra N. Muellner-Riehl for their comments and corrections on an earlier version of the thesis. Thanks go to all my colleagues in Frankfurt and Leipzig, who created a highly pleasant working atmosphere. My special thanks go to Anna-Sarah Becker, Gaelle Bocksberger, Stefan Dressler, Jana Ebersbach, Adrien Favre, Fernando Fernandez-Mendoza, Susanne Fritz, Melanie Grudinski, Frank Hauenschild, Sascha Heller, Christian Hof, Christina Hoppe, Claudia Krueger, Ingo Michalak, 6 Lars Nauheimer, Juraj Paule, Christian Printzen, Pamela Rodriguez, Marco Schmidt, Jan Schnitzler, Daniele Silvestro, and Viola Ziller for great scientific discussions, funny risotto and raclette dinners, several movie and game nights, as well as general support throughout my thesis. Ich möchte auch meinen Eltern, meiner Schwester und ihrem Freund, meinen Großeltern und meinen Freunden für ihre bedingungslose Unterstützung und Liebe danken. Danke, dass ich mich in guten wie in schlechten Zeiten auf euch verlassen kann! Ein besonderer Dank gebührt auch meinem Freund Matthias Renger, der mir über die ganze Doktorarbeitszeit hinweg viel Kraft gegeben hat. Ich danke Dir für so viel Lachen, Trost und Zuspruch! This PhD project was financially supported by the research funding program “LOEWE – Landes-Offensive zur Entwicklung Wissenschaftlich-oekonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts, “Freunde und Foerderer” of Goethe University Frankfurt/Main, the Swiss National Science Foundation, and the German Research Foundation (DFG). 7 TABLE OF CONTENTS LIST OF ABBREVIATIONS ............................................................................. 13 LIST OF FIGURES ........................................................................................... 15 LIST OF TABLES ............................................................................................ 18 1. GENERAL INTRODUCTION ..................................................................... 20 1.1 General aspects of biodiversity and
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