Philodendron Schott (Araceae): Systematics and Evolution of a Mega-Diverse Genus from the New World

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Philodendron Schott (Araceae): Systematics and Evolution of a Mega-Diverse Genus from the New World Philodendron Schott (Araceae): Systematics and evolution of a mega-diverse genus from the New World Inaugural-Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry and Pharmacy of Freie Universität Berlin by Dubán Canal Gallego 2018 1st reviewer: Prof. Dr. Thomas Borsch 2nd reviewer: Prof. Dr. Julien Bachelier Date of disputation: Wednesday, 13th February 2019 ii “Somewhere, something incredible is waiting to be known” Carl Sagan (1934 -1996) iii Acknowledgements Acknowledgements First of all, I am honored to have worked under the supervision of Prof. Dr. Thomas Borsch who provided me the opportunity of conducting this investigation at the Botanischer Garten und Botanisches Museum Berlin - BGBM. Prof. Borsch helped me to design my project and guided me through my studies. I thank Prof. Dr. Julien Bachelier for taking over the role as second reviewer. I am deeply grateful to Dr. Nils Köster, who shared his endless passion for aroids and encouraged me during my studies. Nils joined me during field work in Colombia, gathered a large part of the samples used in this study, introduced me into the Araceae collections at BGBM and discussed various taxonomic issues with me to ensure the correct identification of the respective plants. I further deeply acknowledge the support of Dr. Katy E. Jones during the elaboration of my all analyses. Her discipline, respect and positive attitude inspired me. Katy made me think that science can be surprisingly easy. I especially thank Dr. Nadja Korotkova for her careful revision of my manuscripts and for supporting me all the way up to the submission of my thesis. Thanks further go to Dr. Robert Lücking for his advice when I could only see difficulties and obstacles. I thank Dr. Tom Croat for providing material from the living collection of the Missouri Botanical Garden. As one of the world’s experts on the taxonomy of the Araceae, my sincere thanks for letting me benefit from his knowledge on the morphology and ecology of Philodendron. Thanks go to Carla Kostelac and Alba Luz Arbeláez at the Missouri Botanical Garden for their dedicated support during my visit to St. Louis. During my studies at the BGBM Berlin I attended the Plant Evolution Seminar and the Journal Club offered by my supervisor Prof. Dr. Thomas Borsch and coordinated previously by Dr. Ludo Müller and Dr. Lars Nauheimer and lately by Dr. Katja Reichel and Dr. Michael Grünstäudl, respectively. My investigation benefited from exchanging ideas and sharing concepts with other students, postdoctoral researchers and visitors. These activities contributed significantly to the improvement of my knowledge on plant systematics. This study would not have been possible without the living collections of Philodendron at the BGBM Berlin and the Botanical Gardens of the Universities of Bonn, Göttingen, München, Potsdam, and Wien; the Palmengarten Frankfurt; the Royal Botanic Gardens, Kew, the Missouri Botanical Garden, and the Jardín Botánico José Celestino Mutis in Bogotá. I am iv Acknowledgements therefore deeply grateful to those people whose hands have maintained these collections since many years. The molecular work has been carried out in the molecular laboratory of the BGBM Berlin. I would like to thank the many people who assisted with the laboratory work, in particular Kim Govers, Julia Dietrich, Bettina Giesicke, and Jana Bansemer. Many thanks go to the researchers who I met at the BGBM and who further contributed to an inspiring atmosphere for study, in particular to Dr. Lars Nauheimer, Dr. Katja Reichel, Dr. Grischa Brokamp, Dr. Eckhard von Raab-Straube, Dr. Norbert Kilian, Dr. Tilo Henning, Dr. Susy Fuentes, Dr. Regine Jahn, Gabriele Dröge, and Dr. Brigitte Zimmer. I further thank Dr. Jeannine Marquardt for the German version of the Summary. I am especially grateful to Dr. Rocío Cortés and Dr. Bibiana Moncada from Universidad Distrital Francisco José de Caldas in Bogotá, Dr. Leonardo Palacios curator of the Herbario de la Universidad Tecnológica del Chocó – CHOCO, Dr. Felipe Cardona curator of the Herbario de la Universidad de Antioquia – HUA, Dr. Alejandro Zuluaga from Unversidad del Valle for his support during the field work, and Dr. María Cristina Martínez and Dr. Marcela Celis from Universidad del Norte, for their support during my fieldwork in Colombia. Thanks to all the previous and current staff at the Jardín Botánico José Celestino Mutis for establishing the basis of the scientific cooperation with the BGBM Berlin, in particular Luisz Olmedo Martínez, Dr. Ruth Gutiérrez and Dr. Mauricio Díaz-Granados, and for processing the collections carried out in Colombia and the cooperation in exchanging herbarium material, in particular to César Marín, Ángela Rodríguez y Diana Medellín. I am indebted to the Verein der Freunde des Botanischen Gartens und Botanischen Museums Berlin-Dahlem e.V. for providing financial support for the field work in Colombia. The Bundesministerium für Bildung und Forschung (BMBF) is especially acknowledged for funding a pilot project to facilitate the scientific cooperation between Germany and Colombia (01DN13030). I am deeply grateful to the Deutscher Akademischer Austauschdienst (DAAD) and Colciencias-Colfuturo convocatory 6171 for the financial support. Thanks to all my friends in Colombia and Germany. In Colombia, I am in debt with my dearest Fabio Ávila, Ángela Guzmán, Sandra Ramírez, Javier Garzón, Marcela Castellanos, Mauricio Vargas and Carolina Molano. Your presence in my life has helped me in all senses. In Germany thanks go to my dearest Nana Silakadze, Elmira Maharramova, Demet Töre, Sarah Bollendorf, Ludo Müller, Julie Piérart, Valentina Guissi, Kristýna Šemberová, Jonathan Pahl, Teresa Ortuño, Astrid de Mestier, Mariasole Calbi, Elham Hatami, Arsen Gasparyan and Phnong Thao Nguyen. v Acknowledgements Mil gracias a mis queridos amigos latinoamericanos por haber enriquecido mi vida con tantas experiencias durante mi estadía en Berlín. Martín de León McMannis, Junia Fatorelli, Luciano Tepper, Emmanuel Reyna, Francisco Robles, Rose Álvarez, Vastiane Tamayo, Gerardo Brand, Helena Hernández, Alejandra Baltazares, Rodolfo Paniagua, Nazario López y Nélida Abarca. Mi eterna gratitud a mi familia por ser la razón de todo lo que hago. A mis padres, Inés y Guillermo, gracias siempre. Finally, thanks Gregory d’Hoop for bringing music to my noisy mind. vi Summary Summary This investigation presents phylogenetic analyses of the genus Philodendron, the second largest genus of the “aroid family” and one of the most conspicuous components of Neotropical rainforests. The evolutionary relationships among Philodendron and the closely related genera Adelonema and Homalomena have remained ambiguous based on previous phylogenetic studies that analyzed plastid and nuclear DNA markers for a limited species coverage. Likewise, the evolutionary relationships among the three subgenera proposed within Philodendron (Meconostigma, Philodendron and Pteromischum) remained unclear. Subgenus Meconostigma comprises 21 mostly terrestrial, arborescent species distributed in Amazonia, the Cerrado, and the Mata Atlântica. Subgenus Pteromischum includes 82 appressed-climbing vine species distributed mostly in Central America, the Chocó ecoregion and Amazonia. Subgenus Philodendron accounts for ~85% of the species diversity of the genus, mainly distributed in Central America, the Chocó ecoregion, the Andes and Amazonia. The extraordinary rich species diversity of subgenus Philodendron is currently organized in 10 sections, 12 subsections, and 11 series. The aim of the present study is to elucidate the phylogenetic relationships of Philodendron and its evolutionary history in the Neotropics. Therefore, a molecular dataset of three non-coding plastid DNA regions (petD, rpl16 and trnK/matK) was generated for 173 taxa (221 accessions) across the entire genus Philodendron. Subsequently, the phylogenetic relationships and monophyly of the subgenera were investigated by tree inferences using parsimony-based, maximum likelihood, and Bayesian-based approaches. In order to determine evolutionary time points of the origin of the most recent ancestor and the species diversification process of Philodendron, the well resolved and robustly supported phylogenetic tree was calibrated. Furthermore, analyses on diversification rate shifts through time and inferences of the geographic range evolution were conducted. In addition, the impact of the Andean orogeny on speciation, extinction and dispersal rates of Philodendron was assessed using geographic state-speciation and extinction model analysis. Finally, five morphological characters were analyzed across the phylogenetic tree to infer the ancestral character states. The results indicate that Philodendron and its three subgenera Meconostigma, Philodendron and Pteromischum are monophyletic. However, the relationships among the three subgenera remain moderately supported. The 12 clades recovered within subgenus vii Summary Philodendron do not correspond to the current infrageneric classification. In contrast, clades recovered within subgenus Pteromischum correspond to the sections proposed. Divergence- time estimates revealed that Philodendron originated in the Oligocene, and diversified more recently from the middle Miocene onwards. Time-dependent diversification rate shift analyses revealed that the diversification process of Philodendron combines elements of the two models used to explain the origin of the extraordinary
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