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A Dissertation Entitled Evolution, Systematics A Dissertation Entitled Evolution, systematics, and phylogeography of Ponto-Caspian gobies (Benthophilinae: Gobiidae: Teleostei) By Matthew E. Neilson Submitted as partial fulfillment of the requirements for The Doctor of Philosophy Degree in Biology (Ecology) ____________________________________ Adviser: Dr. Carol A. Stepien ____________________________________ Committee Member: Dr. Christine M. Mayer ____________________________________ Committee Member: Dr. Elliot J. Tramer ____________________________________ Committee Member: Dr. David J. Jude ____________________________________ Committee Member: Dr. Juan L. Bouzat ____________________________________ College of Graduate Studies The University of Toledo December 2009 Copyright © 2009 This document is copyrighted material. Under copyright law, no parts of this document may be reproduced without the expressed permission of the author. _______________________________________________________________________ An Abstract of Evolution, systematics, and phylogeography of Ponto-Caspian gobies (Benthophilinae: Gobiidae: Teleostei) Matthew E. Neilson Submitted as partial fulfillment of the requirements for The Doctor of Philosophy Degree in Biology (Ecology) The University of Toledo December 2009 The study of biodiversity, at multiple hierarchical levels, provides insight into the evolutionary history of taxa and provides a framework for understanding patterns in ecology. This is especially poignant in invasion biology, where the prevalence of invasiveness in certain taxonomic groups could be related to their evolutionary history. In this dissertation, I examined the systematics, phylogeography, population genetics, and biogeography of a group of Ponto-Caspian endemic gobies that includes multiple introduced species in Europe and North America. In Chapters 2 and 4 I found highly divergent genetic lineages within two morphologically defined species (Neogobius fluviatilis and Proterorhinus marmoratus) that are widespread throughout the Ponto- Caspian region. Statistical analyses of morphology identified significant differences according to genetic lineage within each morphospecies, indicating species level divergence among regional taxa. In Chapter 3 I constructed the phylogeny of the Ponto- iii Caspian gobies, finding broad paraphyly in Neogobius sensu Miller & Vasil'eva (2003), and identifying a novel relationship between the “neogobiin” gobies (Babka, Mesogobius, Neogobius, Proterorhinus, and Ponticola) and the tadpole gobies (Anatirostrum, Benthophiloides, Benthophilus, Caspiosoma) as a distinct group highly divergent from other gobiids. I redefined the taxonomy and nomenclature according to the molecular phylogeny, and redescribed the subfamily Benthophilinae to comprise all Ponto-Caspian endemic gobies. In all three chapters, I estimated divergence times among genetic lineages at multiple taxonomic levels, and found gross concordance between the timing of diversification events within the Ponto-Caspian gobies and major geologic changes in the evolution of the Ponto-Caspian basin. Additionally, in Chapters 2 and 4, I identified potential source locations in the northwestern Black Sea for introduced goby populations in northern/central Europe and North America. This dissertation highlights the use of molecular tools to identify cryptic genetic diversity within morphological similar taxa, as well as the role that geologic evolution of the Ponto-Caspian basin has played in shaping the diversity and evolution of its component fauna. iv Acknowledgments Like the proverbial child and the village required for its upbringing, a dissertation is not simply the product of a sole person's effort but results from the combined efforts of a multitude of people who, through their support (academic, financially, or emotionally), help the doctoral student usher to life this new addition to human knowledge. Many have helped me during the course of my dissertation, and my gratitude to them shows no bounds. First and foremost is my adviser Dr. Carol Stepien, whose chance seating next to me at an American Society of Ichthyologists and Herpetologists social event started me along this journey. Thank you for providing the opportunity, support, and resources to allow me to succeed, and for always encouraging me to do so even when I thought that I could not. Thanks as well go to my advisory committee: Drs. Juan Bouzat, David Jude, Christine Mayer, and Elliot Tramer. Your helpful comments, thoughts, and criticisms throughout the course of this work are greatly appreciated, and your multiple different viewpoints always challenged me to think differently about this work. Many thanks go to the former and present students and staff in the Great Lakes Genetics Laboratory: Diana Brandon, Joshua Brown, Amanda Haponski, Ian Hoffman, Rachael Lohner, Doug Murphy, Jennifer Ohayon, Lindsey Pierce, Osvaldo Sepulveda- Villet, and Dr. Rex Strange. All of you have provided valuable discussions and technical assistance, and furnished me with much needed camaraderie and comic relief throughout my laboratory tenure. Thanks go to Ryan Argo, Betsy Bodamer, Kristen DeVanna, Brian Elkington, Ann Krause, Kerry McKenna, Stacy Philpott, Gwen Tenney, and Mike Weintraub for enriching my time at the Lake Erie Center and in the department with their v friendship, and especially to Todd Crail for his friendship and for rapidly dispelling all of my preconceptions about the flora and aquatic fauna of the Midwest. Numerous people in both North America and Europe contributed samples to this work, including: N. Bogutskaya, V. Boldyrev, J. Brown, L. Corkum, I. Grigorovich, J. Herler, S. Ibrahimov, H. Jenner, D. Jude, T. Kakareko, J. Kornichuk, V. Kováč, Y. Kvach, A. Naseka, D. Pratt, S. Rudnicka, M. Sapoto, P. Simonovic, Y. Slynko, A. Smirnov, and C. Wiesner. Access to museum specimens was graciously provided by N. Bogutskaya, G. Burgess, J. Lungberg, D. Nelson, C. Wellendorf, and J. Williams. V. Boldyrev and E. Vasil'eva provided assistance with specimen identification. N. Bogutskaya, W. Eschmeyer, J. Nelson, and E. Vasil'eva provided valuable and thoughtful discussions about the phylogeny and taxonomy presented in Chapter 3, as well as a whirlwind education on the International Code of Zoological Nomenclature rules. Copious technical assistance and chili peppers were provided by Doug Murphy. I am especially indebted to Patricia Uzmann for administrative assistance, and without whom nothing would really ever get done at the Lake Erie Center. Goby collections in Michigan and Ohio were performed under the auspices of scientific collecting permits from the Department of Natural Resources of each state. Several analyses for Chapter 4 were carried out using the resources of the Computational Biology Service Unit from Cornell University, which is partially funded by Microsoft Corporation. Funding for this work was provided by a National Science Foundation grant (DEB-0456972 and REU supplement #0620942) to Carol Stepien, and NSF DeepFin Student Exchange Program award (RCN-0443470 under G. Orti). Thanks go to my parents and family for their love and support throughout my seemingly endless years in graduate school. Final thanks go to my wife, Laura Bedinger: vi your constant love and support despite the time and distance between us during this dissertation is awe-inspiring, and I cannot begin to thank you enough. Much love, kudzu. This dissertation has been brought to you by the letters G, O, B, and Y, and the number 5. vii Table of Contents Abstract...............................................................................................................................iii Acknowledgments................................................................................................................v Table of Contents..............................................................................................................viii List of Tables.......................................................................................................................xi List of Figures....................................................................................................................xii Preface..............................................................................................................................xiii Chapter 1: Introduction........................................................................................................1 Systematics, phylogeography, and biogeography......................................................1 The Ponto-Caspian region..........................................................................................3 The Ponto-Caspian endemic gobies (Gobiidae: Teleostei)........................................5 Objectives ..................................................................................................................6 Chapter 2: Evolution and phylogeography of the tubenose goby genus Proterorhinus (Gobiidae: Teleostei): Evidence for new cryptic species.....................................................8 Abstract...........................................................................................................................8 Introduction.....................................................................................................................9 Methods.........................................................................................................................13 Specimen collection..................................................................................................13
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