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The Population Genetic Structure of Quadrula Aurea (Bivalvia: Unionidae), a Threatened Freshwater Mussel in Central Texas

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The Population Genetic Structure of Quadrula Aurea (Bivalvia: Unionidae), a Threatened Freshwater Mussel in Central Texas THE POPULATION GENETIC STRUCTURE OF Quadrula aurea (BIVALVIA: UNIONIDAE), A THREATENED FRESHWATER MUSSEL IN CENTRAL TEXAS Jeffrey A. Mabe Dissertation Prepared for the Degree of DOCTOR OF PHILOSOPHY UNIVERSITY OF NORTH TEXAS May 2018 APPROVED: James Kennedy, Major Professor Jeff Johnson, Committee Member David Hoeinghaus, Committee Member Miguel Acevedo, Committee Member Art Goven, Committee Member and Chair of the Department of Biological Sciences Su Gao, Dean of the College of Science Victor Prybutok, Dean of the Toulouse Graduate School Mabe, Jeffrey A. The Population Genetic Structure of Quadrula aurea (Bivalvia: Unionidae), A Threatened Freshwater Mussel in Central Texas. Doctor of Philosophy (Biology), May 2018, 148 pp., 23 tables, 19 figures, references, 230 titles. The anthropogenic alteration of riverine ecosystems has led to declines in the abundance and diversity of freshwater mussels (Bivalvia: Unionoida) worldwide. Central Texas is home to a diverse freshwater mussel fauna including three candidates for federal listing under the Endangered Species Act. Surveys conducted over the last few decades suggest many of the endemic freshwater mussel species in Texas exist in small isolated populations that may be vulnerable to the deleterious effects of genetic diversity loss. Microsatellite primers from two closely related species were used to identify a set of genetic markers that functioned in the golden orb (Quadrula aurea). Microsatellite markers were then applied to document the population genetic structure of Q. aurea within and among three connected river drainages in southeastern Texas. Gene flow within existing Q. aurea populations appears high indicating little potential for genetic issues stemming from isolation and inbreeding. Two weakly divergent admixed populations were identified occupying the San Antonio and Guadalupe/San Marcos rivers. Population genetic structure was related to river basin affiliation, but results for environmental factors were unresolved. Current effective population size estimates are large for the Guadalupe/San Marcos drainage and moderately large for the San Antonio drainage and there is no clear genetic evidence of contemporary population declines. Transport in the glochidial phase by a highly mobile host fish, the channel catfish (Ictalurus punctatus), may provide a mechanism for maintaining connectivity among spatially discrete mussel beds and deserves further study. Information on the occurrence and habitat associations of Q. aurea and two other threatened freshwater mussel species was documented. Quantification of the population genetic structure for Q. aurea provides important information needed for the management of this species, a baseline for understanding future changes, and insight into the factors that shape the population genetic structure of other threatened unionids in Texas. Copyright 2018 By Jeffrey A. Mabe ii ACKNOWLEDGEMENTS Thank you to my major advisor Dr. James Kennedy for allowing me to pursue this research, guiding me through the education experience, and providing the funding support needed to complete this project. Thanks also to Sigma Xi the Scientific Research Honor Society for providing grant support. A special thank you is owed to Dr. Jeff Johnson and his graduate students Sarah Schulwitz and Susan Hammerly who provided invaluable guidance in the principles of conservation genetics and the techniques for DNA extraction, PCR amplification, and analysis of genetic data. Thank you to my entire committee (Dr. Kennedy, Dr. Jeff Johnson, Dr. David Hoeinghaus, Dr. Kelly Reyna, and Dr. Miguel Acevedo) for the guidance and insight you provided. Thank you to my friends and family for supporting me in this effort. To my mom: you taught me patience and perseverance and never let me forget I could accomplish anything I set my mind to. To my dad: you helped instill in me a drive for the pursuit of intellectual achievement that changed the course of my life. And finally to my Wife, Heather: your love, support, and patience erased any self-doubt and gave me the confidence to complete this task. I would like to thank the following people who have offered assistance and helped to fulfill the goals of this project: Dr. Kevin Roe (Iowa State University), who provided microsatellite primers, genetic sequences for Quadrula fragosa, and guidance in mussel sampling techniques; Robert Howells (Biostudies, Kerrville Texas), who provided specimen verification for Quadrula aurea, Quadrula petrina, and Fusconaia mitchelli; Dr. Nathan Johnson (US Geological Survey), who provided information on host fish species for Q. aurea. iii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ................................................................................................................... iii LIST OF TABLES ............................................................................................................................... vii LIST OF FIGURES .............................................................................................................................. ix CHAPTER 1. INTRODUCTION ........................................................................................................... 1 1.1 Statement of Problem ............................................................................................. 1 1.2 Objectives and Hypotheses..................................................................................... 4 1.2.1 Objectives .................................................................................................... 4 1.2.2 Null Hypotheses .......................................................................................... 4 1.3 Scope ....................................................................................................................... 5 CHAPTER 2. BACKGROUND AND LITERATURE REVIEW .................................................................. 6 2.1 Distribution and Conservation Status of Freshwater Bivalves ............................... 6 2.2 Importance of Genetic Diversity ............................................................................. 8 2.3 Genetic Structure, Spatial Structure, and River Fragmentation ........................... 10 2.4 Population Size ...................................................................................................... 14 2.5 Mussel Distribution and Habitat Associations ...................................................... 15 CHAPTER 3. METHODOLOGY ........................................................................................................ 21 3.1 Mussel Surveys ...................................................................................................... 21 3.2 Habitat Measurements ......................................................................................... 23 3.3 Genetic Sample Collection and Processing ........................................................... 29 3.4 Primer Testing ....................................................................................................... 30 3.5 Power Analysis of Microsatellite Markers ............................................................ 32 3.6 Analyses of Population Genetic Structure ............................................................ 33 3.6.1 Detection of Genotyping Errors ................................................................ 34 3.6.2 Genetic Diversity ....................................................................................... 35 3.6.3 Genetic Structure ...................................................................................... 35 3.6.4 Assignment Test ........................................................................................ 37 iv 3.6.5 Spatial and Environmental Influence on Genetic Structure ..................... 38 3.7 Demographic History and Effective Population Size (Ne) ..................................... 41 CHAPTER 4. RESULTS ..................................................................................................................... 45 4.1 Survey Results ....................................................................................................... 45 4.2 Habitat Measurements ......................................................................................... 48 4.2.1 Habitat Measurements: Statistical Relations among River Basins ........... 50 4.2.2 Habitat Measurements: Spearman Correlation ........................................ 53 4.2.3 Habitat Measurements: Principle Components Analysis.......................... 54 4.3 Marker Identification ............................................................................................ 57 4.3.1 Loci Characteristics .................................................................................... 59 4.3.2 Power Analysis .......................................................................................... 61 4.4 Q. aurea Genetic Structure ................................................................................... 61 4.4.1 Neutral Genetic Diversity .......................................................................... 61 4.4.2 Genetic Structure ...................................................................................... 65 4.4.3 Assignment Test ........................................................................................ 68 4.5 Population Size ...................................................................................................... 69 4.6 Influence of Spatial and Environmental Factors
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