Molecular Investigations of the Diversity of Freshwater Fishes Across Three Continents
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Molecular Investigations of the Diversity of Freshwater Fishes across Three Continents by Malorie M. Hayes A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama August 8, 2020 Keywords: Enteromius, Barbus, sub-Saharan Africa, phylogenetics, systematics, Pteronotropis, conservation genetics, Trichomycterus, Guyana Copyright 2020 by Malorie M. Hayes Approved by Jonathan W. Armbruster, Chair, Professor and Director Auburn University Museum of Natural History Department of Biological Sciences Jason E. Bond, Professor and Schlinger Chair in Insect Systematics University of California, Davis Scott R. Santos, Professor and Chair of the Department of Biological Sciences at Auburn University John P. Friel, Director of the Alabama Museum of Natural History Abstract Fishes are the most speciose vertebrates, and incredible diversity can be found within different groups of fish. Due to their physiological limitations, fish are confined to waters, and in freshwater fish, this is restricted to lakes, rivers, and streams. With a constrained habitat like a freshwater system, it can be expected that freshwater fish will show varying levels of diversity depending on a suite of characteristics. Within this dissertation, I examine the diversity of three fish groups: the speciose Enteromius of West Africa, the population genetic diversity of Pteronotropis euryzonus in Alabama and Georgia, and the unexpectedly species rich Trichomycterus from the Guyana highlands. I use molecular methods and geometric morphometrics to determine the systematics of the species and uncover the hidden diversity within their respective groups. When it comes to diversity, the small barbs of Africa are vastly understudied and require a taxonomic revision. From that revision, a better understanding of the diversity leads to a new genus description. For the small-bodied minnow Pteronotropis, moving across a river was believed to be unlikely. Highland catfishes like Trichomycterus were believed to be limited not only in their dispersal ability, but also in their diversity. The diversity of freshwater fishes is reflected within the chapters of this dissertation. ii Acknowledgements This research was funded through the ACSII NSF Grant DEB-1023403. In addition to funding, these projects would have never been completed without my collaborators, helpers, lab-mates, and friends. Thanks to Hank Bart, Albert Chakona Ray Schmidt, and Melanie Stiassny for providing tissues. For help with the Pteronotropis chapter, I thank J. Williams, B. Albanese, J. Holcomb, B. Kuhadja and A. George, B. Gould. Trichomycterus projects are possible through the help of Donald Taphorn, Nathan Lujan, Larry Page, and Elford Liverpool as well as Aiesha Williams and Chuck Hutchinson of the Guyana WWF. Ovid Williams, Patamona people of Kaibarupai, Ayangana, and Chenapowu, Mark Sabaj, Luz Ochoa, Erling Holm. Thanks to H. L. Bart, Jr., S. Diallo, T. Diallo, L. Fitzgerald, J. P. Friel, M. Magase, C. K. Ray, R. C. Schmidt, N. Smolensky, M. Sou, C. C. Stout, J. Sullivan, J.-P. Thumitho, A. Walanga, and K. Winemiller for collection efforts. A special thank you to Kyle Luckenbill for photographing specimens. Many thanks to Brian Sidlauskas for providing the tissues and samples, to Joe Cutler, Gervais Koudaou, Mve Beh, and Jean Hervé for their work in the field to collect the specimens, Thanks to Erika Krahl and Kasey Benesh for their molecular techniques and skills. Lab-mates are invaluable for their friendships and input. Thanks David Werneke, Lesley de Souza, Shobnom Ferdous, C. Keith Ray, Milton Tan, Carla Stout, Ed Burress, Pam Hart, Tobit Liyandja, Courtney Weyand, Corinthia Black, Daniel Akin and lab adoptee, Charles Stephen. Thanks to my undergraduate mentees, Erika Krahl, Kathlene Joyce, and Holden Paz, who helped me find motivation when it was lacking. Thanks to the spider people and lab-mates, Chris Hamilton, Vera Opatova, Juanita Rodriguez, Rebecca Godwin, Kellie Bourguinon, and Nicole Garrison. Thanks, herp people and lab- mates Jamie Oaks, Kerry Cobb, JR Wood, and Charlotte Benedict. My dissertation committee was incredibly important in helping me focus my goals, push me to be a better scientist, and support me along the path to PhD. Thanks Jon, Jason, John, and Scott. A final thanks to my family, whose support has been so consistent. I love you, Lillian, for all the joy you bring to my life. And a special thanks to the single most important person to my success. He has underwritten all travel expenses, supported me in my times of weakness, given me space to learn and grow as a researcher and as a person, listened when I rambled about fishes and trees, and loved me every step of the way. Thank you, Jacob Barger. iii Table of Contents Abstract ............................................................................................................................... ii Acknowledgements ............................................................................................................ iii Table of Contents ............................................................................................................... iv List of Tables ..................................................................................................................... vi List of Figures ................................................................................................................... vii Chapter 1 – Introduction .................................................................................................. 1-1 Chapter 2 – The Taxonomy and Relationships of the African Small Barbs (Cypriniformes: Cyprinidae) ................................................................................ 2-1 Abstract ................................................................................................................ 2-1 Introduction .......................................................................................................... 2-1 Materials and Methods ......................................................................................... 2-4 Results .................................................................................................................. 2-7 Discussion .......................................................................................................... 2-12 Figures................................................................................................................ 2-17 Tables ................................................................................................................ 2-19 Chapter 3 – A new genus of minnow in West Africa (Cypriniformes, Cyprinidae, Smiliogastrini)...................................................................................................... 3-1 Abstract ................................................................................................................ 3-1 Introduction .......................................................................................................... 3-1 Methods................................................................................................................ 3-4 Results .................................................................................................................. 3-6 Discussion .......................................................................................................... 3-11 Figures................................................................................................................ 3-17 Chapter 4 – Conservation Genetics of the Broadstripe Shiner, Pteronotropis euryzonus, an Endemic to the Middle Chattahoochee River ................................................. 4-1 Abstract ................................................................................................................ 4-1 Introduction .......................................................................................................... 4-2 Materials and Methods ......................................................................................... 4-6 Results ................................................................................................................ 4-10 Discussion .......................................................................................................... 4-13 Figures................................................................................................................ 4-21 iv Tables ................................................................................................................ 4-26 Chapter 5 – A Hotspot Atop: Rivers of the Guyana Highlands Hold High Diversity of Endemic Pencil Catfish (Teleostei: Ostariophysi: Siluriformes) ......................... 5-1 Abstract ................................................................................................................ 5-1 Introduction .......................................................................................................... 5-2 Materials and Methods ......................................................................................... 5-6 Results .................................................................................................................. 5-9 Discussion .......................................................................................................... 5-11 Figures...............................................................................................................