Evolutionary History of Floral Key Innovations in Angiosperms Elisabeth Reyes

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Evolutionary History of Floral Key Innovations in Angiosperms Elisabeth Reyes Evolutionary history of floral key innovations in angiosperms Elisabeth Reyes To cite this version: Elisabeth Reyes. Evolutionary history of floral key innovations in angiosperms. Botanics. Université Paris Saclay (COmUE), 2016. English. NNT : 2016SACLS489. tel-01443353 HAL Id: tel-01443353 https://tel.archives-ouvertes.fr/tel-01443353 Submitted on 23 Jan 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. NNT : 2016SACLS489 THESE DE DOCTORAT DE L’UNIVERSITE PARIS-SACLAY, préparée à l’Université Paris-Sud ÉCOLE DOCTORALE N° 567 Sciences du Végétal : du Gène à l’Ecosystème Spécialité de Doctorat : Biologie Par Mme Elisabeth Reyes Evolutionary history of floral key innovations in angiosperms Thèse présentée et soutenue à Orsay, le 13 décembre 2016 : Composition du Jury : M. Ronse de Craene, Louis Directeur de recherche aux Jardins Rapporteur Botaniques Royaux d’Édimbourg M. Forest, Félix Directeur de recherche aux Jardins Rapporteur Botaniques Royaux de Kew Mme. Damerval, Catherine Directrice de recherche au Moulon Président du jury M. Lowry, Porter Curateur en chef aux Jardins Examinateur Botaniques du Missouri M. Haevermans, Thomas Maître de conférences au MNHN Examinateur Mme. Nadot, Sophie Professeur à l’Université Paris-Sud Directeur de thèse M. Sauquet, Hervé Maître de conférences à l’Université Invité (co-directeur de Paris-Sud thèse) ACKNOWLEDGEMENTS I thank my thesis supervisors Sophie and Hervé for their help, as well as the other members of the EVA team, but most particularly the people I saw regularly such as Julien, Frank, Stefan, Laetitia, Renske, Qian, Charlotte, James, Véronique and Thierry. I also thank people from outside the team that have contributed to my papers such as Hélène Morlon, Jürg Schönenberger and Maria von Balthazar. I thank the jury Louis Ronse de Craene, Félix Forest, Catherine Damerval, Porter Lowry, and Thomas Haevermans to have taken time to evaluate my thesis and participate in the defense. I thank the member of my thesis committee for advising me: Susana Magallón, Marianne Elias, Jean-Yves Dubuisson. I also thank Jacqui and Martine for having helped me with my various paperwork worries and the other people I got to meet during my stay in this lab. I thank my parents and officemates Roxane, Julie and Angeline for their moral support. 2 TABLE OF CONTENTS ACKNOWLEDGEMENTS ..................................................................................................... 2 TABLE OF CONTENTS ......................................................................................................... 3 GENERAL INTRODUCTION ............................................................................................... 4 1. The many faces of the flower ................................................................................................................... 4 2. A series of abominable mysteries ............................................................................................................ 6 3. The neglected flip side of the abominable mystery.................................................................................. 9 4. The critical role of ancestral state reconstruction in the study of character evolution ........................... 10 5. Thesis objectives .................................................................................................................................... 11 CHAPTER 1: Presence in Mediterranean hotspots and floral symmetry affect speciation and extinction rates in Proteaceae ........................................................................................ 13 ABSTRACT .............................................................................................................................................. 18 INTRODUCTION ..................................................................................................................................... 19 MATERIALS AND METHODS ............................................................................................................... 22 RESULTS .................................................................................................................................................. 26 DISCUSSION ............................................................................................................................................ 30 ACKNOWLEDGEMENTS ....................................................................................................................... 37 CHAPTER 2: Perianth symmetry changed at least 199 times in angiosperm evolution 38 ABSTRACT .............................................................................................................................................. 42 INTRODUCTION ..................................................................................................................................... 43 MATERIALS AND METHODS ............................................................................................................... 44 RESULTS .................................................................................................................................................. 47 DISCUSSION ............................................................................................................................................ 57 ACKNOWLEDGMENTS ......................................................................................................................... 71 CHAPTER 3: Does heterogeneity of rates of morphological evolution affect ancestral state reconstructions? An empirical test with five floral characters ................................. 72 ABSTRACT .............................................................................................................................................. 76 INTRODUCTION ..................................................................................................................................... 77 MATERIALS AND METHODS ............................................................................................................... 79 RESULTS .................................................................................................................................................. 84 DISCUSSION ............................................................................................................................................ 90 GENERAL DISCUSSION ................................................................................................... 100 Properties of trees created by “change-capturing” transitions in binary characters ................................. 101 Elements missing to better understand the diversification of angiosperms ............................................. 106 CONCLUSION AND PERSPECTIVES ............................................................................ 112 LITERATURE CITED ........................................................................................................ 115 SUPPORTING INFORMATION ....................................................................................... 130 3 GENERAL INTRODUCTION 1. THE MANY FACES OF THE FLOWER The flower is a short axis bearing, from the center out, female reproductive organs consisting of ovules protected by carpels, male reproductive organs called stamens and a perianth (Bateman et al. 2006). The flower is one of the most distinctive features of angiosperms, the clade of land plants with the highest diversity. “Diversity” is here used in the sense of having a large number of species, and is accompanied by a variety of flower forms that is exemplified in Figure I.1. The image that the word “flower” evokes to the layman probably greatly resembles the upper left picture of Figure I.1 and consists of reproductive organs of both sexes surrounded by a specialized two-whorl perianth in which the inner whorl is colorful and showy but delicate, while the outer whorl is more inconspicuous and stiff as it protects the developing bud; it will also probably have five petals and five sepals. That mental picture includes the organs being separate and those of a given category being the same size and shape. Adaptation to pollinators, self-pollination, abiotic pollination or simply evolutionary history has led to the development among flowers of aspects that are radically different from that “layman’s mental image”. For instance, the “sepal and petal” perianth is not the only form of perianth that exists and is actually a derived state (see Figure I.3 and Chapter 3). Species from the early-diverging clades of angiosperms can have only one type of perianth part, or two types that are different in shape but of similar color, petal-like or sepal-like. Flowers from these early- diverging clades can also have more than two perianth whorls or a spiral perianth, usually associated with a large number of perianth parts. While most species in such cases are found in early-diverging angiosperms, the above situations occasionally appear within clades in which the “sepal and
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