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Elaphoglossum Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie der Ludwig-Maximilians-Universität München EVOLUTION AND CLASSIFICATION OF ELAPHOGLOSSUM AND ASPLENIUM FERNS ON CUBA, AND DISCOVERY OF A MIOCENE ELAPHOGLOSSUM IN DOMINICAN AMBER Josmaily Lóriga Piñeiro München, 15. Januar 2018 ii A mi familia y mis amigos, donde quiera que estén To my family and my friends, wherever they are iii iv PREFACE Statutory declaration Erklärung Diese Dissertation wurde im Sinne von §12 der Promotionsordnung von Prof. Dr. Jochen Heinrichs betreut. Ich erkläre hiermit, dass die Dissertation nicht einer anderen Prüfungskommission vorgelegt worden ist und dass ich mich nicht anderweitig einer Doktorprüfung ohne Erfolg unterzogen habe. Eidesstattliche Erklärung Ich versichere hiermit an Eides statt, dass die vorgelegte Dissertation von mir selbstständig und ohne unerlaubte Hilfe angefertigt wurde. Josmaily Lóriga, 15. Januar 2018 (Unterschrift) 1. Gutachter: Prof. Dr. Susanne S. Renner 2. Gutachter: Prof. Dr. Reinhard Agerer Tag der Abgabe: 15. Januar 2018 Tag der Disputation: 28. Februar 2018 v vi Declaration of contribution In this thesis, I present the results from my doctoral research, carried out in Munich from March 2013 to January 2018 (maternity leave between February and December 2017) under the guidance of Prof. Dr. Jochen Heinrichs. My thesis resulted in three published manuscripts presented in Chapters 2 to 4. I generated all data and conducted all analyses myself with some exceptions: Chapter 2, Alejandra Vasco produced Fig. 4; Chapter 3, Ledis Regalado conducted the study of gametophytes and generated the drawings of Fig. 1; and Chapter 4, Kathrin Feldberg contributed to the divergence time estimates and Alexander R. Schmidt produced Fig. 1. Writing and discussion involved collaboration with J. Heinrichs, with input from the co-authors. Josmaily Lóriga Prof. Susanne S. Renner (Signature) (Signature) List of publications Peer-reviewed journal articles LÓRIGA, J., VASCO, A., REGALADO, L., HEINRICHS, J., MORAN, R.C. 2014. Phylogeny and classification of the Cuban species of Elaphoglossum (Dryopteridaceae), with description of Elaphoglossum sect. Wrightiana sect. nov. Plant Systematics and Evolution 300, 937–951. LÓRIGA, J., SCHMIDT, A.R., MORAN, R.C., FELDBERG, K., SCHNEIDER, H., HEINRICHS, J. 2014. The first fossil of a bolbitidoid fern belongs to the early- divergent lineages of Elaphoglossum (Dryopteridaceae). American Journal of Botany 101, 1466–1475. LÓRIGA, J., REGALADO, L., PRADA, C., SCHNEIDER, H., HEINRICHS, J. 2016. Phylogenetic relationships of two Cuban spleenworts with unusual morphology: Asplenium (Schaffneria) nigripes and Asplenium pumilum (Aspleniaceae, leptosporangiate ferns). Plant Systematics and Evolution 303, 165–176. vii Funding My research was supported by a Research Assistant position at the Faculty of Biology of the University of Munich (LMU) between 1 March and 31 May 2013; a fellowship from the Deutscher Akademischer Austauschdienst (DAAD) from 1 September 2013 until 31 August 2016, the Christopher Reynold Foundation and the International Association for Plant Taxonomy. viii CONTENTS Preface ....................................................................................................................................... v Statutory Declaration ................................................................................................... v Erklärung ..................................................................................................................... v Eidesstattliche Erklärung ............................................................................................. v Declaration of contribution ....................................................................................... vii List of publications ................................................................................................... vii Funding .................................................................................................................... viii Contents...................................................................................................................................ix Summary...................................................................................................................................1 Chapter 1: General Introduction............................................................................................... 3 1.1 Elaphoglossum: Phylogeny and morphology ........................................................ 6 1.2 Systematics and Evolution of Asplenium .............................................................. 9 1.3 The fossil record in ferns ..................................................................................... 10 1.4 Research questions ............................................................................................... 12 Chapter 2: Phylogeny and classification of the Cuban species of Elaphoglossum (Dryopteridaceae), with description of Elaphoglossum sect. Wrightiana sect. nov. ..................................................................................................................... 14 Chapter 3: Phylogenetic relationships of two Cuban spleenworts with unusual morphology: Asplenium (Schaffneria) nigripes and Asplenium pumilum (Aspleniaceae, leptosporangiate ferns) ...................................................................................... 32 Chapter 4: The first fossil of a bolbitidoid fern belongs to the early-divergent lineages of Elaphoglossum (Dryopteridaceae) ..................................................................... 47 Chapter 5: General Discussion ............................................................................................... 71 5.1 Phylogeny and classification of Cuban Elaphoglossum and Asplenium ............. 73 5.1.1 Elaphoglossum .................................................................................................. 73 5.1.2 Asplenium ......................................................................................................... 74 5.2 The inclusion of Elaphoglossum in Miocene Dominican amber ......................... 76 5.3 General conclusion and perspective .................................................................... 77 References ............................................................................................................................... 79 Acknowledgements ................................................................................................................ 87 Curriculum vitae .................................................................................................................... 89 ix x SUMMARY This dissertation deals with the systematics and evolution of Neotropical ferns of the genera Elaphoglossum and Asplenium, with particular focus on the species of Cuba and the West Indies. It also includes an analysis and description of an Elaphoglossum frond fragment preserved in Miocene Dominican amber. The worldwide genera Elaphoglossum with 600 species and Asplenium with 685 species are the most species-rich groups of leptosporaniate ferns. On Cuba, Elaphoglossum has 34 species and Asplenium 32. I performed phylogenetic analyses of plastid DNA sequence matrices that included almost 300 sequences of Elaphoglossum and its closest outgroups, with especially dense sampling of the Cuban Elaphoglossum, mostly newly sequenced during my research. The Cuban endemic E. wrightii was found to be an early-diverging lineage of Elaphoglossum, not a member of section Squamipedia in which it had previously been classified; I therefore created a separate section for this species. This species climbs upwards on the lower portions of tree trunks but never loses its connection with the soil while most remaining species of Elaphoglossum retain no connection to the soil and are holo-epiphytes. The plastid DNA phylogeny in combination with an in-depth analysis of the morphology of West Indian Elaphoglossum allowed me to confidently assign a fern inclusion from Miocene Dominican amber to the genus by reconstructing the evolution of relevant morphological characters (preserved in the fossil) on the molecular phylogeny of extant taxa. The infrageneric classification of Asplenium is notoriously difficult as a result of extensive morphological homoplasy and plasticity. Molecular-phylogenetic studies have shed light on major lineages within Asplenium including some morphologically highly distinct species. Among these is Asplenium nigripes, a species occurring in Costa Rica, Guatemala, and Cuba where it grows on rocks in mountain forests between 900 and 1500 m. The species is unusual in having entire suborbicular to rhomboid fleshy blades that do not look like typical fern fronds. My molecular phylogenetic analysis revealed that it is the sister species to A. pumilum, also occurring on Cuba but with ‘normal’ fern leaves except for unusual whitish hairs. Using micro-morphological leaf and spore traits, I tried to find additional support for a close relationship of these two species, but was unable to detect any synapomorphies, which highlights both the importance of molecular characters for investigating species relationships in Asplenium and our still incomplete knowledge of the phenotypic traits of Cuban ferns. 1 2 Chapter 1 GENERAL INTRODUCTION 3 4 Islands have been of disproportionate importance to the study of evolution since the voyages of Charles Darwin to the
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