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Phylogenetic Systematics of the Supragenus Rasbora (Teleostei: Cyprinidae)

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Phylogenetic Systematics of the Supragenus Rasbora (Teleostei: Cyprinidae) Phylogenetic Systematics of the Supragenus Rasbora (Teleostei: Cyprinidae) by Daniel Natanael Lumbantobing B.S. in Biology, December 2004, Universitas Indonesia, Depok, Indonesia A Dissertation submitted to The Faculty of Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy January 31, 2013 Dissertation directed by John R. Burns Professor of Biology Lynne R. Parenti Research Scientist, National Museum of Natural History, Smithsonian Institution The Columbian College of Arts and Sciences of The George Washington University certifies that Daniel Natanael Lumbantobing has passed the Final Examination for the degree of Doctor of Philosophy as of November 29, 2012. This is the final and approved form of the dissertation. Phylogenetic Systematics of the Supragenus Rasbora (Teleostei: Cyprinidae) Daniel Natanael Lumbantobing Dissertation Research Committee: John R. Burns, Professor of Biology, Dissertation Co-Director Lynne R. Parenti, Research Scientist, National Museum of Natural History, Smithsonian Institution, Dissertation Co-Director Guillermo Ortí, Louis Weintraub Associate Professor of Biology, Committee Member Richard P. Vari, Research Scientist, National Museum of Natural History, Smithsonian Institution, Committee Member ii © Copyright 2012 by Daniel Natanael Lumbantobing All rights reserved iii Dedication To my home-archipelago, Indonesia, and its people… To my loving parents: my late father Nukman Lumban Tobing, for his constant presence, despite being no longer with us, that constantly reverberates in my thought as a great person, and most importantly, his momentous encouragement, despite his non-scientific background, that helped me to set my life fixed on becoming a biologist; such a “serendipitous path” that I had never thought of pursuing during my fledgling pre-college years (and neither had he then); and my mother, Siti Mariam Manoppo, whose passionate care, relentless patience, and devoted encouragement keep nourishing me with hope and optimism. …Science is perhaps one gigantic jigsaw puzzle game with its countless pieces; the puzzle that tells us about the nature of our own universe… I wish to always just be a player of this stunning game... who can assemble a few of its puzzling pieces into a bigger picture, thus, to contribute more to our understanding about this universe… who, at the end of the day, may sip his cup of tea while enjoying a portion of the universe’s masterpiece through the everlasting scholarly records… ~Depok, Indonesia, 2004 iv Acknowledgments The seven year process of making this dissertation would not have been possibly completed without the help, support, and encouragement of many great individuals, to whom I hereby wholeheartedly acknowledge. I would like to thank my co-advisors, Lynne Parenti and John Burns, for their insightful knowledge and wisdom, let alone their unwavering patience in giving me the guidance to understand what and how science is, and also the encouragement through all ups and downs during these past seven years. It has been indeed an absolute privilege and a great pleasure to have both of them as my scientific supervisors. I would like to express my gratitude to the members of my dissertation committee for their time, perspectives, and constructive criticisms. I thank Richard Vari and Guillermo Ortí whose feedback has been very instrumental in shaping the final version of this dissertation as well as my training as an ichthyologist. I am grateful to Patricia Hernandez and Eric Hilton for their constructive criticisms in improving this dissertation. I am also grateful to all the professors in the Department of Biological Sciences at GWU, especially to Diana Lipscomb, Gustavo Hormiga, and James Clark. Also, a number of people to whom I am indebted for their expertise, technical supports and contributions, without which this dissertation would not have been finalized as it is. I deeply appreciate and acknowledge some people in the Fish Division, Smithsonian Institution, for their help: Jeff Williams, Jeff Clayton, Sandra Raredon, Kris Murphy, and Jerry Finan. For lengthy scientific discussion and insightful knowledge, I am indebted with Renny Hadiaty, Maurice Kottelat, Prosanta Chakrabarty, Ralf Britz, v Tan Heok Hui, Kevin Tang, Larry Page, Kevin Conway, Dave Johnson, John Sparks, Peter Konstantinidis, and Nalani Schnell. For assistance during the field work, I thank Renny Hadiaty, Deden Rudaya, Ni Made Rai, Archimedes Daely, and Heri Chin. For tissue samples and specimen loan, I thank Renny Hadiaty, Tan Heok Hui, Lukas Rüber, Kevin Tang, Hendra Budianto, Mark Sabaj Perez, Rob Robbins, Kelvin Lim, Patrick Campbell, Oliver Crimmen, Barbara Brown, Martin Van Oijen, Ronald de Ruiter, Ronald Vonk, and Hielke Praagman. Lee Weigt kindly permitted access to the Laboratory of Analytical Biology (LAB) of Smithsonian Institution. I thank people in LAB who kindly assisted me in solving problems of molecular labwork: Jeff Hunt, Gabe Johnson, Andrea Ormos, and Maggie Halloran. Many thanks to all my friends for all the supports, intellectual sharing and great friendship during the process of finishing this dissertation: Renny Widjojo, Vinita Gowda, Maria Rosario Castañeda, Deden Rudaya, Rob Javonillo, Ryuji Machida, Heri Chin, Cristiano Moreira, Ximo Mengual, Matthieu Leray, Jeffrey Sosa, Katie Staab, Fiona Wilkinson, Dan Mulcahy, Amanda Windsor, Ligia Benavides, and Ehsan Kayal. I am grateful to my relatives in DC for the caring support: Anton Manoppo, Ifa Ishak, Emmy Hoover, Bambang Suroso, Monalisa Bambang, Fari Nasution, Mayang Nasution, Ira Istarina, and Bramanda Arioboma. Finally, last but not least, to my family who are always with me: my late father (Nukman Lumban Tobing), mother (Siti Mariam Manoppo), my brothers and sister (Sinar Anton Lumbantobing, Anita Triani Tobing, and M. Ery Syahruni). This dissertation research was funded by the Herbert R. and Evelyn Axelrod Fund and the Leonard P. Schultz Funds from the Division of Fishes, Smithsonian Institution; vi the Weintraub Fellowship in Biological Sciences of GWU; a fieldwork grant from All Catfish Species Inventaory (ACSI); and the Student Exchange Program from the DeepFin Project 2007. vii Abstract of Dissertation Phylogenetic Systematics of the Supragenus Rasbora (Teleostei: Cyprinidae) The fishes of the supragenus Rasbora, with 104 valid species, comprise among the most species-rich and widespread lineages of cyprinids that live throughout a vast expanse from the subcontinent India through Southeast Asia as far south as Sundaland. Despite its remarkable diversity, high abundance, and broad distribution, the systematics of Rasbora is highly problematic primarily due to the conflicting phylogenetic hypotheses among previous studies. A multifaceted systematic study incorporating more taxa and characters of Rasbora, which encompasses the alpha-taxonomic work of Rasbora as well as phylogenetic analyses using both morphology and molecules, was conducted to resolve the current systematic disagreement and taxonomic problems of the group. The alpha-taxonomic study in the present study results in the description of eight new species of Rasbora from northern Sumatra: Rasbora api, R. kluetensis, R. nodulosa, R. truncata, Rasbora n. sp. 1, Rasbora n. sp. 2, Rasbora n. sp. 3, and Rasbora n. sp. 4. In addition, a new set of characters useful to diagnose for two rasborin groups, the Reticulata and Sumatrana groups, were described (i.e., the microstructure of the cephalic tubercles and the body pigmentations). Given the allopatric distribution of three of the aforementioned new species, three areas of endemism in northwestern Sumatra are recognized. Cladistic analysis of Rasbora was performed using a dataset containing 274 morphological characters coded for 97 taxa (70 ingroups, 27 outgroups) under the maximum parsimony algorithm, which resulted in a total of 3,411 most parsimonious trees with 1,111 steps length (CI = 0.42; RI 0.57; RI = 0.88; RC = 0.37). The topology of the viii consensus tree recovered the monophyly of the supragenus Rasbora with high nodal support and five unique synapomorphies. Twelve major monophyletic lineages corresponding to the previously recognized supraspecific groups of Rasbora were recovered in the topology, each of which with moderate to strong nodal support and with a set of unreversed synapomorphies. Moreover, the monophyly of several featured cyprinid taxa is supported with a series of novel unreversed synapomorphies: (1) the subfamily Danioninae; (2) the clade Danionini+Rasborini; (3) the tribe Chedrini; (4) the tribe Danionini; and (5) the tribe Rasborini. Seven genetic markers, which are four nuclear genes (EPIC 55305, EPIC 35692, RAG1, and Rhodopsin) and three mitochondrial regions (16S rRNA, COI, and cytochrome b) sequenced from 93 taxa (80 ingroups, 13 outgroups) were used in the present molecular analyses. The phylogenetic trees were reconstructed based on several different datasets (i.e., individual markers, concatenated datamatrix with different partitioning scenarios) under three general phylogenetic algorithms (maximum parsimony, maximum likelihood, and Bayesian inference). Overall, the three different phylogenetic approaches result in trees with similar topologies of the backbone, in which two major clades of the tribe Rasborini are recovered consistently with high support values: (1) the Indian lineage (12 species), and (2) the Sundaland-Indochinese lineage (92 species). Similar to
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