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Evolution, Speciation, and Conservation of Amblyopsid Cavefishes

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Evolution, Speciation, and Conservation of Amblyopsid Cavefishes University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 8-2011 Evolution, Speciation, and Conservation of Amblyopsid Cavefishes Matthew Lance Niemiller [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Evolution Commons Recommended Citation Niemiller, Matthew Lance, "Evolution, Speciation, and Conservation of Amblyopsid Cavefishes. " PhD diss., University of Tennessee, 2011. https://trace.tennessee.edu/utk_graddiss/1106 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Matthew Lance Niemiller entitled "Evolution, Speciation, and Conservation of Amblyopsid Cavefishes." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Ecology and Evolutionary Biology. Benjamin M. Fitzpatrick, Major Professor We have read this dissertation and recommend its acceptance: James A. Fordyce, Randall L. Small, Matthew J. Gray Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) To the Graduate Council: I am submitting herewith a dissertation written by Matthew Lance Niemiller entitled “Evolution, speciation, and conservation of amblyopsid cavefishes.” I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the requirements for the degree of Doctor of Philosophy, with a major in Ecology and Evolutionary Biology. Dr. Benjamin Fitzpatrick, Major Professor We have read this dissertation and recommend its acceptance: Dr. James Fordyce Dr. Randall Small Dr. Matthew Gray Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official student records.) Evolution, Speciation, and Conservation of Amblyopsid Cavefishes A Dissertation Presented for The Doctor of Philosophy Degree The University of Tennessee, Knoxville Matthew Lance Niemiller August 2011 Copyright © 2011 by Matthew Lance Niemiller All rights reserved. ii ACKNOWLEDGEMENTS This dissertation would not have been completed without the guidance, advice, mentoring, and support of my advisor Ben Fitzpatrick. I could not have asked for a better advisor, mentor, and friend. I am particularly grateful to my committee comprised of Jim Fordyce, Randy Small, and Matt Gray for their encouragement and mentorship. I must also include Darrin Hulsey, Brian Miller, Tom Near, and Brian O’Meara as “unofficial” committee members. All of these individuals have influenced me greatly in not only the way I view and conduct science, but my development and ultimate success as a scientist in academia. I am forever indebted to all of you. I must thank other faculty and staff in the Department of Ecology and Evolutionary Biology who assisted, encouraged, and supported me during my time at UTK, including Phyllis Bice, Chris Boake, Jaime Call, Sandy Echternacht, Dave Etnier, Pearl Kirkland-Smith, Cheryl Lynn, Gary McCracken, Anne Mintz, and Nate Sanders. I owe special thanks to the cave biologists who have come before me and advanced the field. Particularly, I thank the late Tom Barr, John Cooper, John Holsinger, Jerry Lewis, Tom Poulson, and Daphne Soares for their insightful discussions, assistance, and encouragement during my dissertation. I also must thank all my family and friends who have offered considerable support and encouragement throughout my thirteen (yes thirteen) years of college. I must thank many individuals outside of UTK for their assistance on various aspects of this dissertation, including access to caves, fieldwork, molecular work, and discussion: Ginny Adams, Jon Armbruster, Jen Buhay, Geoff Call, Jim Cooley, Amy Crews, Spike iii Crews, Dylan Dittrich-Reed, Joe Douglas, Jody Eberly, Bill Elliott, Dante Fenolio, Lee Florea, Bill Gee, Brad Glorioso, Jim Godwin, Geo Graening, Sue Hagan, Phillip Hollingsworth, Scott House, Andy Isbell, John Jensen, Ron Johnson, Denise Kendall, Bernie Kuhajda, Randy Long, Thany Mann, Zach Marion, John McCormack, Roger McCoy, Karen Mobley, Avise Moni, Gerald Moni, Rick Olson, Dave Neely, Trent Niemiller, Jeff Page, Stesha Pasachnik, Bill Pearson, R. Graham Reynolds, Jason Robinson, Al Romero, Premal Shah, Larry Simpson, Daphne Soares, Mick Sutton, Mark Thurman, Jason Todd, Kevin Toepke, Rick Toomey, Brian Wagner, Bill Walden, Pic Walenta, Shawn Williams, David Withers, Richie Wyckoff, and several others who I’ve unintentionally omitted. I must thank several organizations for permits, allowing access to caves on their properties, or logistical support, including: Mammoth Cave National Park, Ozark National Scenic Riverways, United States Fish and Wildlife Service, Mark Twain National Forest, Alabama Department of Conservation and Natural Resources, Arkansas Game and Fish Commission, Indiana Department of Natural Resources, Georgia Department of Natural Resources, Kentucky Department of Fish and Wildlife Resources, Missouri Department of Conservation, Missouri Department of Natural Resources, Tennessee Department of Environment and Conservation, Tennessee Wildlife Resources Agency, National Speleological Society, Alabama Cave Survey, Kentucky Speleological Survey, Missouri Speleological Survey, Tennessee Cave Survey, Carroll Cave Conservancy, Cave Research Foundation, Southeast Cave Conservancy, Nature Conservancy, and many private landowners. iv Funding for this dissertation was provided in part by the Tennessee Wildlife Resources Agency, Kentucky Department of Fish and Wildlife Resources, Department of Biology at Middle Tennessee State University, Department of Ecology and Evolutionary Biology at the University of Tennessee-Knoxville, Department of Ecology and Evolutionary Biology at Yale University, National Science Foundation (DDIG to MLN; award no. DEB-1011216), American Museum of Natural History, Cave Research Foundation, Institute for a Secure and Sustainable Environment, American Society of Ichthyologists and Herpetologists, and National Speleological Society. v ABSTRACT Cave organisms are classic examples of regressive evolution, as many disparate taxa have evolved similar convergent phenotypes in subterranean environments. While recent phylogeographic and population genetic analyses have greatly improved our understanding of the evolutionary and biogeographic history of cave organisms, many questions remain unanswered or poorly investigated. I investigated several evolutionary and biogeographic questions in a model system for regressive evolution and studies of ecological and evolutionary mechanisms, amblyopsid cavefishes. In chapter I, I used recently developed methods to delimit species boundaries and relationships in a widely distributed cavefish, Typhlichthys . I show that species diversity in Typhlichthys is currently underestimated and that the view of a single, widely distributed species is not valid. Rather, several morphologically cryptic lineages comprise the diversity in this clade. In chapter II, I examined regressive evolution and potential re-evolution of an eyed, surface form in amblyopsid cavefishes. Whether evolution is truly irreversible, known as Dollo’s Law, has become a question of increasing interest, as several recent studies have made claims that complex structures can be recovered after loss. Phylogenetic and ancestral character state analyses of amblyopsid cavefishes are consistent with re-evolution of eyes and pigmentation and recolonization of surface habitats in the surface-dweller Forbesichthys , providing an opportunity to rigorously discriminate between re-evolution and parallel evolution of cave phenotypes. Despite strong support for re-evolution and contradiction of Dollo’s Law, eye histological vi evidence and analyses of molecular evolution in the eye gene rhodopsin are consistent with Dollo’s Law supporting at least three independent subterranean colonizations and eye degeneration. Phylogenetic reconstructions of character evolution can occasionally produce strongly supported yet misleading results. In chapter III, I examined the biogeography and speciation of Typhlichthys . Phylogenetic and divergence time analyses support monophyly of Typhlichthys with the majority of cladogenic events occurring in the late Pliocene to Pleistocene, implicating climate change as the primary mechanism driving diversification. Biogeographical analyses, examination of molecular variation in rhodopsin , and structuring of genetic variation with hydrological boundaries, support multiple colonization events by a broadly distributed surface ancestor that subsequently went extinct rather than a single colonization event followed by subterranean dispersal and vicariance. vii TABLE OF CONTENTS ACKNOWLEDGEMENTS ............................................................................................iii ABSTRACT ...................................................................................................................... vi GENERAL INTRODUCTION .......................................................................................
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