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Phylogeny of the Family Eunicidae (Polychaete, Annelida) Based on Molecular and Morphological Data

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PHYLOGENY OF THE FAMILY EUNICIDAE (POLYCHAETE, ANNELIDA) BASED ON MOLECULAR AND MORPHOLOGICAL DATA by Joana Zanol Pinheiro da Silva Teaching License in Biology, 1999, Universidade Federal do Rio de Janeiro, Brazil Master in Science-Zoology, 2002, Universidade Federal do Rio de Janeiro, Brazil 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, 2009 Dissertation directed by Diana Leigh Lipscomb Professor of Biology Kristian Fauchald Research Zoologist, NMNH The Columbian College of Arts and Sciences of The George Washington University certifies that Joana Zanol Pinheiro da Silva has passed the Final Examination for the degree of Doctor of Philosophy as of November 18, 2008. This is the final and approved form of the dissertation. PHYLOGENY OF THE FAMILY EUNICIDAE (POLYCHAETE, ANNELIDA) BASED ON MOLECULAR AND MORPHOLOGICAL DATA Joana Zanol Pinheiro da Silva Dissertation Research Committee: Diana Leigh Lipscomb, Professor in Biology, Co-Director Kristian Fauchald, Research Zoologist, NMNH, SI, Co-Director Sheri A. Church, Assistant Professor of Biological Sciences, Committee Member James M. Clark, Ronald B. Weintraub Professor of Biology, Committee Member ii © Copyright 2008 by Joana Zanol Pinheiro da Silva All rights reserved iii Dedication To my parents and sister for the unconditional support always. ”Nothing in life is to be feared. It is only to be understood” Marie Curie “An expert is a man who has made all the mistakes which can be made in a very narrow field” Niels Bohr iv Acknowledgments This work would not have been possible without the help, support and guidance of many people to whom I am greatly thankful. Foremost, I would like to thank both of my advisors Dr. Diana L. Lipscomb and Dr. Kristian Fauchald for the support, guidance and freedom for independent thinking and for allowing me to pursue my own ideas throughout this research. I am also thankful to Dr. Kristian Fauchald for believing in me from my undergraduate years, which pushed me forward and made this graduate experience possible. I would like to thank the members of my dissertation committee, Dr. Sheri A. Church, Dr. James M. Clark, Dr. Gustavo Hormiga and Dr. Allen G. Collins, for the discussions during the course of the research, the critical review of this work and helpful suggestions that made it better, and for coping with tight schedules. I am grateful to Dr. Kenneth M. Halanych for his essential contribution throughout this work and technical support with the molecular bench work; and Dr. Torsten H. Struck for sharing unpublished data and information and for the help in my first steps in the molecular laboratory. All professors, students and staff of the Department of Biological Sciences at GWU were of great importance during this work. I am greatly thankful to them, especially the systematics course professors, Dr. Marc W. Allard, Dr. James M. Clark, Dr. Patrick S. Herendeen and Dr. Gustavo Hormiga, whose courses provided me with important knowledge to carry out this research; Dr. Fernando Alvarez, M. Rosario Castañeda, Vinita Gowda, Lara Lopardo and Dr. Dimitar Dimitrov, for the very fruitful informal discussion v on systematics; M.Rosario Castañeda and Vinita Gowda, also for the very valuable comments on the preview of my dissertation seminar; Dr. Patricia Hernandez and Nathan Bird, for the comments on the confocal laser scanning microscopy results; Dr. Hartmut G. Doebel and the late Paul Spiegler for the very valuable guidance through the Teaching Assistant experience; Dr. John R. Burns and Dr. James M. Clark for being engaged graduate advisors; Rashelle Shanon and Hoda Fatah for going out of their way to help; and Dr. Matjaz Kuntner, Dr. Ingi Agnarsson and Dr. Svetlana Maslakova, for the tips on the graduate life at GWU and in the United States. I am also greatly thankful to all the staff in Invertebrate Zoology Department at Natural History Museum, Smithsonian Institution, especially Dr. Jon Norenburg, for providing important information for field work; Linda Ward, W. Geoff Keel, William Moser, Paul R. Greenhall, Tim Coffer and Cheryl Bright, for the help with my research and for dealing with all the loans necessary for this project. I am extremely grateful to all the staff and post-doctorate fellows at the Smithsonian Marine Station at Fort Pierce, which made it possible to complete the work for Chapter 2 in a short period of time and for making my stay in Fort Pierce very pleasant. I am especially thankful to Dr. Mary Rice, Dr. Valerie Paul, Sherry Reed, Michael Scott Jones, Julie Piraino, William (Woody) Lee, Hugh Reichardt and Joan Kaminski for all their help. I am pleased to thank Dr. George von Dassow for the introduction and invaluable help with confocal laser scanning microscopy; Dr. Anja Schulze for important help with confocal laser scanning microscopy techniques; Scott Whittaker, for his unconditional help in all steps of Scanning Electron Microscopy (SEM); Lara Lopardo, for the introduction to SEM; Nataliya Budaeva for the identification of onuphids; Dr. Christoph Bleidorn, Dr. vi Tiago B. Quental, Dr. Omar Torres-Carvajal for discussions on phylogenetic analyses; Dr. Kevin de Queiroz for discussion of various systematics topics and for giving me access to his computers; Dr. Paulo C. Paiva, for constant encouragement, for dealing with Brazilian collecting permits, and for giving me access to his laboratory; Dr. Alexander Tzetlin, for the comments on the confocal laser scanning microscopy results; Diana Marques for the help with graphic softwares; Dr. Leonard Hirsch for constant encouragement, information on collecting permits and general discussions; and all members in Dr. Halanych’s lab in the Spring 2005, especially Heather Blasczyk, Dr. Lee Weight, Jeff Hunt, Dr. Jeff Bates, and all other members of the LAB, NMNH, Smithsonian Institution. Institution, without whom the molecular laboratory work would not have been possible. This work would not have been possible without the extensive donation and loan of specimens by several people from diverse institutions, for this reason I am indebted to Dr. M. Teresa Aguado (Universidad Autónoma de Madrid, Spain), Dr. Christos Arvanitidis (Hellenic Centre for Marine Research, Greece), Dr. Nicola Bettoso (Osservatorio Alto Adriatico ARPA-FVG, Italy), Dr. Luis F. Carrera-Parra (El Colegio de la Frontera Sur, Mexico), Dr. Danny Eibye-Jacobsen (Zoological Museum, Copenhagen, Denmark), Dr. Maria Cristina Gambi (Stazione Zoologica Anton Dohrn, Italy), Dr Chris Glasby (Northern Territory Museum, Australia), Dr. Bert Hoeksema (National Natural History Museum Naturalis Leiden, Netherlands), Dr. Stéphane Hourdez (Station Biologique de Roscoff, France), Dr. Ardis Johnston (Harvard Univeristy, USA), Dr. Stephen Keable (Australian Museum, Australia), Dr. Ceri Lewis (University of the Western Cape, South Africa), Dr. Eduardo López (Universidad Autónoma de Madrid, Spain), Linda Meurisse (Institut Royal Des Sciences Naturelles de Belgique, Belgium), Dr. Tarik Meziane (Musée National vii d'Histoire Naturelle, France), Dr. Birger Neuhaus (Museum für Naturkunde der Humboldt- Universität zu Berlin, Germany), Anderson Oliveira (Universidade do Estado do Rio de Janeiro, Brazil), Dr. Julio Parapar (Universidade da Coruña, Spain), Dr. Fredrik Pleijel (Tjärnö Marine Biological Laboratory, Göteborg University, Sweden), Dr. Alexandra Rizzo (Museu de Zoologia da Universidade de São Paulo, Brazil), Dr. Anja Schulze, (Texas A&M University, Galveston Campus, Texas), Dr. Emma Sherlock (The Natural History Museum, United Kingdom), Dr. Elin Sigvaldadottir (The Swedish Museum of Natural History, Sweden), Roger Springthorpe (Australian Museum, Australia), Leonne Vermond (National Natural History Museum Naturalis Leiden, Netherlands), Dr. Miguel Villena (Museo Nacional de Ciencias Naturales, Spain), Sara C. Watson (America Museum of Natural History, USA) and Gisela Weigel (Zoologisches Museum, Universität Hamburg, Germany). I am also indebted with all those who helped in the sampling of the specimens used here, Leslie H. Harris, Dr. Bruno Pernet, Shelly Walther, David E. Montagne, John, all the staff in the July 2004 monitoring cruise of the County Sanitation District of Los Angeles County, Dr. Rosebel C. Nalesso, Wilson Franklin Junior, Rossana Sousa, Tatiane Martins Garcia, Dr. Flavia Mochel, Jane, Luiz, other UFMA undergraduate students, Dr Martin Christoffersen, Andre Souza, Sherry Reed, Michael Scott Jones, William (Woody) Lee, Natalyia Budaeva, Geoff Keel, Dr. Fredrik Pleijel and Dr.Greg Rouse. These collections would not have been possible without the kind hospitality of Leslie H. Harris, David Ocker, Liliane Zanol, Bernardo and Júlia Zanol Xavier. viii I extend my thanks to all friends and extended family, who were very important providing emotional support and encouragement, especially Vinita Gowda, Diana Marques, Simone S. O. Pszczol, Tiago B. Quental, Christine Ruta and Paulo C. Paiva. Finally, I would like to thank my parents for the constant invaluable support and for setting the grounds of whom I am today, always encouraging me to follow my dreams and, to work for the things I want; my sister for always being there, believing in me and encouraging me to move forward; and my late beloved grandma, who was very puzzled with what I was doing but nevertheless very proud of it. This research was funded by a NSF doctoral dissertation improvement grant, NSF-
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  • Neanthes Limnicola Class: Polychaeta, Errantia

    Neanthes Limnicola Class: Polychaeta, Errantia

    Phylum: Annelida Neanthes limnicola Class: Polychaeta, Errantia Order: Phyllodocida, Nereidiformia A mussel worm Family: Nereididae, Nereidinae Taxonomy: Depending on the author, Ne- wider than long, with a longitudinal depression anthes is currently considered a separate or (Fig. 2b). subspecies to the genus Nereis (Hilbig Trunk: Very thick segments that are 1997). Nereis sensu stricto differs from the wider than they are long, gently tapers to pos- genus Neanthes because the latter genus terior (Fig. 1). includes species with spinigerous notosetae Posterior: Pygidium bears two, styli- only. Furthermore, N. limnicola has most form ventrolateral anal cirri that are as long as recently been included in the genus (or sub- last seven segments (Fig. 1) (Hartman 1938). genus) Hediste due to the neuropodial setal Parapodia: The first two setigers are unira- morphology (Sato 1999; Bakken and Wilson mous. All other parapodia are biramous 2005; Tusuji and Sato 2012). However, re- (Nereididae, Blake and Ruff 2007) where both production is markedly different in N. limni- notopodia and neuropodia have acicular lobes cola than other Hediste species (Sato 1999). and each lobe bears 1–3 additional, medial Thus, synonyms of Neanthes limnicola in- and triangular lobes (above and below), called clude Nereis limnicola (which was synony- ligules (Blake and Ruff 2007) (Figs. 1, 5). The mized with Neanthes lighti in 1959 (Smith)), notopodial ligule is always smaller than the Nereis (Neanthes) limnicola, Nereis neuropodial one. The parapodial lobes are (Hediste) limnicola and Hediste limnicola. conical and not leaf-like or globular as in the The predominating name in current local in- family Phyllodocidae. (A parapodium should tertidal guides (e.g.