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Rabeling 2010 Dissertation Copyright by Christian Rabeling 2010 The Dissertation Committee for Christian Rabeling certifies that this is the approved version of the following dissertation: Diversity and evolution of reproductive systems in Mycocepurus fungus-gardening ants Committee: Ulrich G. Mueller, Supervisor Daniel I. Bolnick David M. Hillis Theodore R. Schultz Michael C. Singer Diversity and evolution of reproductive systems in Mycocepurus fungus-gardening ants by Christian Rabeling, Dipl. Biol. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin May, 2010 Dedication To my parents, Renate and Klaus Rabeling, for unconditionally fostering my curiosity and my love for biological sciences, and to my fiancée, Simone Caroline Cappellari, whose love and support seem inexhaustible. Acknowledgements A doctoral dissertation is not an accomplishment of a single person. Throughout my studies I was fortunate to have experienced the guidance of several outstanding advisors, mentors and friends. I would like to sincerely thank: my advisor, Ulrich Mueller, for providing an inspiring academic environment, encouraging my independent research efforts, and enthusiastically supporting me as a student in his laboratory; the members of my committee, Ulrich Mueller, Dan Bolnick, David Hillis, Ted Schultz and Mike Singer, for providing stimulating discussions and constructive criticism; my mentors outside UT Austin, Stefan Cover, Manfred Verhaagh, and Phil Ward, for being a reliable source of inspiration and friendship. I owe gratitude to many folks for enriching my social and academic life throughout the dissertation process: John Abbott, Rachelle Adams, Nikhil Advani, Deepa Agashe, Karin Akre, Sabrina Amador, Natalia Biani, Jeremy & Erin Brown, Eric Caldera, Evan Economo, Catalina Estrada, Nicole Gerardo, Eben Gering, Will Harcombe, Anna Himler, Henrik Hjarvard de Fine Licht, Vicky Huang, Heather Ishak, Katrin Kellner, Krushnamegh Kunte, Emily McTavish, Sandy Monahan, Greg Pauly, Samraat Pawar, Rainer Radtke, Andre Rodrigues, Jon Seal, Becky Symula, Pam Willis, and Sze Huei Yek; and especially Scott Solomon and Sasha Mikheyev for being great lab mates and valued friends, and my friend, office mate, and fellow Entomology TA, Barrett Pupated Klein, entomo-artist extraordinaire. I also wish to thank Gary Alpert, Maurício Bacci Jr., Barry Bolton, Koos Boomsma, Sean Brady, Beto Brandão, Guy Bush, Jim Carpenter, Lloyd Davis, Mark Deyrup, Rodrigo Feitosa, Fernando Fernández, Brian Fisher, Jürgen Gadau, Marcos Garcia, Bert Hölldobler, Bob Johnson, John Lattke, Jack Longino, Bill Mackay, v Sergio Sanchez-Peña, the late Roy Snelling, Walter Tschinkel, Alex Wild, and Ed Wilson for their (myrmecological) collegiality and generous aid. I was fortunate to have the help of talented and enthusiastic undergraduate research assistants and gratefully acknowledge Misha Blizard, Dev Dash, Rosemary French, Omar Gonzales, Jenny Ji, Paul Roncal, and Hong Thai. Most significantly, I thank my fiancée, Simone Caroline Cappellari, for understanding my passion and her loving support during this exciting period of our lives. The second chapter has been previously published in PLoS ONE (2009, 4(8): e6781) with José Lino-Neto, Simone Cappellari, Iracenir Santos, Ulrich Mueller, and Maurício Bacci, Jr as co-authors. We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for permission to conduct fieldwork in Brazil. We are grateful to Beto Brandão (MZSP), Stefan Cover (MCZ), Ted Schultz (NMNH) and Heraldo Vasconcelos (UFU) for contributing specimens to our study. We also thank the staff of the Reserva Ecológica do IBGE for support during fieldwork. We would like to thank Natalia Biani, Stefan Cover, Barrett Klein, Sasha Mikheyev, Jon Seal, Kazuki Tsuji, and Phil Ward for commenting on earlier versions of this manuscript, and four anonymous reviewers for constructive criticism. The third chapter is based on a manuscript that will be submitted for publication and is co-authored by Omar Gonzales, Maurício Bacci Jr., Marcos Garcia, Ted Schultz, and Ulrich G. Mueller. We are grateful to the following scientists and institutions for generously providing access to specimens and study sites: Beto Brandão (MZSP), James Carpenter (AMNH), Stefan Cover, Gary Alpert and Edward O. Wilson (MCZC), Fernando Fernández (Universidad Nacional de Colombia, Bogotá, Colombia), Jorge Luis Fontenla (Academia de Ciencias de Cuba), Augusto Henriques (INPA), John Lattke (Museo del Instituto de Zoología Agrícola vi ‘Francisco Fernández Yépez’, Maracay, Venezuela), Jack Longino (INBC, JTCL), William MacKay (WPMC), Jean-Michel Maes (Museo Entomológico, León, Nicaragua), Bernhard Merz (MHNG), Nigel Pitman (Amazon Conservation Association, Peru), Roberto Poggi and Valter Raineri (MCSN), Sergio Sánchez-Peña (Universidad Autónoma Agraria Antonio Narro, Saltillo, Coahuila, Mexico), José Santisteban (Universidad Nacional Agraria La Molina, Lima, Peru), the late Roy Snelling (LACM), Heraldo Vasconcelos (UFU), Manfred Verhaagh (SMNK), Phil Ward (UCDC), Autoridad Nacional del Ambiente and Smithsonian Tropical Research Institute, Panama, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), the Forestry Division and Wildlife Section of Trinidad, the Minesterio del Ambiente y Energia, Costa Rica, and the office of the President of Guyana. David Hillis, Daniel Bolnik and Mike Singer improved the manuscript with helpful comments. CR gratefully acknowledges financial support from Ernst Mayr Travel Grants in Animal Systematics (Museum of Comparative Zoology), the Green Fund (Harvard University), a NSF Doctoral Dissertation Improvement Grant (DEB-0808164), the Explorer’s Club Exploration Fund, a Lewis and Clark Field Scholarship, research grants from the Section of Integrative Biology at the University of Texas at Austin, and a University Continuing Fellowship from UT Austin; MB received support from the Fundação de Apoio à Pesquisa do Estado de São Paulo (2006/00185-7) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (476250/2008-0 and 310826/2006-3); UGM was funded by grants form the NSF (DEB-0808164, DEB-0639879, DEB-0110073, DEB-998379). The fourth chapter is based on a manuscript that has been accepted for publication in Systematic Entomology (2010, in press) and is co-authored by Maurício Bacci Jr. We are grateful to the following curators who generously provided access to the indicated collections: James Carpenter (AMNH), Jack Longino (INBC, JTCL), Augusto Henriques (INPA), the late Roy Snelling (LACM), Roberto vii Poggi and Valter Raineri (MCSN), Stefan Cover and Edward O. Wilson (MCZC), Bernhard Merz (MHNG), Beto Brandão (MZSP), Manfred Verhaagh (SMNK), Sergio Sánchez-Peña (SSPC), Phil Ward (UCDC), Heraldo Vasconcelos (UFU), Ted Schultz (USNM), and William MacKay (WPMC). Koos Boomsma, Stefan Cover, Volker Nehring, Ted Schultz, and Sze Huei Yek provided stimulating discussions about inquiline biology. Johan Billen gave valuable advice for interpreting the glandular orifices of the social parasite. Scott E. Solomon took the photograph of the parasite queen in the artificial nest. Sabrina Amador, Stefan Cover, Heather Ishak, Ulrich Mueller, Sze Huei Yek, and two anonymous reviewers improved the manuscript with their comments. Dwight Romanovicz provided technical support during SEM photography. We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for permission to conduct fieldwork in Brazil. We gratefully acknowledge our funding sources: CR received financial support from an Ernst Mayr Travel Grant in Animal Systematics (Museum of Comparative Zoology), the Green Fund (Harvard University), a NSF Doctoral Dissertation Improvement Grant (DEB-0808164), the Explorer’s Club Exploration Fund, a Lewis and Clark Field Scholarship, and research grants from the Section of Integrative Biology from the University of Texas at Austin; MB received support from the Fundação de Apoio à Pesquisa do Estado de São Paulo (2006/00185-7) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (476250/2008- 0 and 310826/2006-3). viii Diversity and evolution of reproductive systems in Mycocepurus fungus-gardening ants Publication No._____________ Christian Rabeling, Ph.D. The University of Texas at Austin, 2010 Supervisor: Ulrich G. Mueller The general prevalence of sexual reproduction over asexual reproduction among metazoans testifies to the evolutionary, long-term benefits of genetic recombination. Despite the benefits of genetic recombination under sexual reproduction, asexual organisms sporadically occur throughout the tree of life, and a few asexual lineages persisted over significant evolutionary time without apparent recombination. The study of asexual organisms therefore may provide clues to answer why almost all eukaryotes reproduce via meiosis and syngamy and why asexual eukaryotes are almost always evolutionarily short-lived. Towards understanding the evolution of asexual lineages in the Hymenoptera, I first review the diversity of reproductive systems in the Hymenoptera, introduce the study organism, the fungus-gardening
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