University of Missouri, St. Louis IRL @ UMSL Dissertations UMSL Graduate Works 8-3-2011 Understanding the origin and rapid diversification of the genus Anthurium Schott (Araceae), integrating molecular phylogenetics, morphology and fossils Monica Maria Carlsen University of Missouri-St. Louis, [email protected] Follow this and additional works at: https://irl.umsl.edu/dissertation Part of the Biology Commons Recommended Citation Carlsen, Monica Maria, "Understanding the origin and rapid diversification of the genus Anthurium Schott (Araceae), integrating molecular phylogenetics, morphology and fossils" (2011). Dissertations. 414. https://irl.umsl.edu/dissertation/414 This Dissertation is brought to you for free and open access by the UMSL Graduate Works at IRL @ UMSL. It has been accepted for inclusion in Dissertations by an authorized administrator of IRL @ UMSL. For more information, please contact [email protected]. Mónica M. Carlsen M.S., Biology, University of Missouri - St. Louis, 2003 B.S., Biology, Universidad Central de Venezuela – Caracas, 1998 A Thesis Submitted to The Graduate School at the University of Missouri – St. Louis in partial fulfillment of the requirements for the degree Doctor of Philosophy in Biology with emphasis in Ecology, Evolution and Systematics June 2011 Advisory Committee Peter Stevens, Ph.D. (Advisor) Thomas B. Croat, Ph.D. (Co-advisor) Elizabeth Kellogg, Ph.D. Peter M. Richardson, Ph.D. Simon J. Mayo, Ph.D Copyright, Mónica M. Carlsen, 2011 Understanding the origin and rapid diversification of the genus Anthurium Schott (Araceae), integrating molecular phylogenetics, morphology and fossils Mónica M. Carlsen M.S., Biology, University of Missouri - St. Louis, 2003 B.S., Biology, Universidad Central de Venezuela – Caracas, 1998 Advisory Committee Peter Stevens, Ph.D. (Advisor) Thomas B. Croat, Ph.D. (Co-advisor) Elizabeth Kellogg, Ph.D. Peter M. Richardson, Ph.D. Simon J. Mayo, Ph.D Copyright, Mónica M. Carlsen, 2011 ACKNOWLEDGEMENTS I would like to thank my Advisor, Dr. Peter Stevens (University of Missouri – St. Louis), and co-Advisor, Dr. Thomas Croat (Missouri Botanical Garden) for helping me all the way during my graduate studies. I am also thankful to my committee members, Dr. Elizabeth “Toby” Kellogg (University of Missouri – St. Louis) for letting me work in her molecular lab and for very helpful suggestions to improve grant and manuscript writing, Dr. Mick Richardson (Missouri Botanical Garden) for always finding funds to cover my studies, and Dr. Simon Mayo (Royal Botanic Gardens at Kew, England) for sharing his knowledge of the family Araceae with me. I am also deeply grateful to the faculty, curators, staff and graduate students at both the University of Missouri – St. Louis and the Missouri Botanical Garden for their help, discussions, suggestions and friendship. And, very specially, the Kellogg’s lab members, Jan Barber, Mark Beilstein, Paulo Camara, Andrew Doust, Cynthia Hong-Wa, Meredith Jacques, Elma Kay, David Kenfack, Shelby Kleweis, Lucia Lohmann, Simon Malcomber, Anya Penly, Jill Preston, Renata Reinheimer, Patrick Sweeney, Anthony Verboom, Beto Vicentini, Sarah Youngstrom, Felipe Zapata, all of whom help me discover and enjoy the wonders and problems of producing a molecular phylogeny. I would also like to thank the many funding sources that made possible this research through their generous financial support: the National Science Foundation through a Doctoral Dissertation Improvement Grant (# 0709851), the Desmond Lee Fund at the Kellogg’s Lab, the Missouri Botanical Garden, the W. R. Harris World Ecology Center at the University of Missouri -St. Louis, the Botanical Society of America, the American Society of Plant Taxonomists, the Royal Botanical Gardens in Kew, England with a Kew Latin American Research Fellowship, the Garden Club of America, and the International Aroid Society. This study would not have been possible without the help and “green thumb” of Emily Colletti, the Araceae greenhouse manager at the Missouri Botanical Garden, who has taken excellent care of one the best cultivated aroid collections in the world. Approximately 90% of the specimens used in this study came from those greenhouses. Other aroid researchers also contributed to the development of this project with their suggestions, samples and discussions, Anne Swart (while at Washington University – St. Louis), Dr. Lívia Godinho Temponi (Universidade Estadual do Oeste do Paraná, Brazil) and Dr. Natalie Cusimano (Ludwig-Maximilians Universität, München, Germany). I would also like to thank my field assistants in several countries, Dan Levin and Thomas Croat in Ecuador; Carmen Emilia Benítez, Ismael Capote, Alfonso Cardozo, Dumas Conde and Carlos Reyes in Venezuela; and, Hector Gómez, Jorge Martínez, Nayarit Martínez and Miguel Angel Perez-Ferrara in Mexico. I am thankful to all my friends and family, in St. Louis and in Venezuela, that have helped in the long road of my graduate studies, especially to Kuo-Fang Chung, Indiana Coronado, Patty Feria, Sara Fuentes, Jason Krause & family, Rosa Ortiz, John Pruski, Ben Torke, Lupita Sanchez, Homero Vargas. I would love to thank my favorite graphic designer, Rhandus Malpica, for designing my Anthurium logo and for being with me even when I was in another country. And finally, I am in debt with Mauricio Diazgranados for a very important last minute “rescue” when my computer unexpectedly died a week before my Dissertation defense. LIST OF CONTENTS Abstract…………………………………………………………………………………... 1 Chapter 1. A molecular phylogeny of Anthurium Schott (Araceae) based on combined chloroplast and nuclear DNA…………………………………………. 3 Introduction………………………………………………………………………. 4 Materials and Methods…………………………………………………………… 7 Results…………………………………………………………………………... 12 Discussion………………………………………………………………………. 17 Conclusions and Further Research……………………………………………… 27 Literature cited………………………………………………………………….. 30 Figure 1. Split-graph of trnH-psbA sequences of Anthurium…………………... 38 Figure 2. Bayesian consensus tree of combined cpDNA datasets……………… 39 Figure 3. Bayesian consensus tree of combined cpDNA and nDNA datasets….. 40 Table 1. Anthurium species and specimens used in molecular phylogenetic analyses.……………………………………………………………………….... 41 Table 2. Characteristics of cpDNA and nDNA molecular datasets used to reconstruct the phylogeny of Anthurium.………………………………..……... 45 Table 3. Characteristics of the parsimony, likelihood and Bayesian analyses used to reconstruct the phylogeny of Anthurium………………………………. 46 Chapter 2. A revision of the currently accepted sectional classification of Anthurium Schott (Araceae) and its associated morphology based on a molecular phylogeny of the genus……………………………………………. 47 I Introduction……………………………………………………………………... 48 Materials and Methods………………………………………………………….. 50 Results…………………………………………………………………………... 53 Discussion………………………………………………………………………. 56 Conclusions and Further Research……………………………………………… 81 Literature cited………………………………………………………………….. 84 Figure 1. The first of the most-parsimonious trees obtained from parsimony ratchet analyses of combined cpDNA and nDNA sequences of Anthurium…… 90 Figure 2. The best scoring maximum likelihood tree obtained from likelihood analyses of combined cpDNA and nDNA sequences of Anthurium…….……... 91 Figure 3. Character state reconstructions for spadix and fruit color along the Anthurium molecular phylogeny……………………………………………. 92 Table 1. A comparison of the main sectional classification systems of Anthurium to date……………………………………………………………. 93 Table 2. Currently accepted sectional classification of Anthurium…………….. 95 Table 3. Morphological characters previously used in the sectional classification of Anthurium……………………………………………………... 96 Table 4. Morphological matrix of Anthurium species sampled in this study………………………………………………………………………... 97 Table 5. Results of hypothesis testing of topological differences among likelihood and parsimony phylogenetic hypothesis using Shimodaira-Hasegawa and Templeton’ tests…………………………………………………………... 101 Table 6. Parameters of the reconstruction of morphological characters II in Anthurium…………………………………………………………………... 102 Appendix 1. Reconstruction of morphological characters along the phylogeny of Anthurium………………………………………………………. 103 Chapter 3. Origin and diversification of the genus Anthurium Schott (Araceae) through time…………………………………………………………………… 116 Introduction……………………………………………………………………. 117 Materials and Methods………………………………………………………… 119 Results…………………………………………………………………………. 125 Discussion……………………………………………………………………... 128 Conclusions and Further Research…………………………………………….. 137 Literature cited………………………………………………………………… 140 Figure 1. Araceae phylogeny with age estimates for relevant clades.………… 146 Figure 2. Anthurium phylogeny with age estimates for relevant clades………. 147 Table 1. Estimated ages (in million years ago - Mya) of nodes in the Araceae-phylogram……………………………………………………………. 148 Table 2. Estimated ages (in million years ago - Mya) of nodes in the Anthurium-phylogram…………………………………………………………. 150 III ABSTRACT Anthurium is a strictly neotropical genus of Araceae ranging from southern Mexico to northern Argentina, including ca. 900 species and displaying an enormous variation in leaf morphology, growth habit, leaf venation pattern and inflorescence and fruit colors. Despite its immense diversity, its ecological importance in Neotropical forests, and a very long history of botanical collection, cultivation, and taxonomical research, Anthurium had been almost neglected in molecular phylogenies.