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A Dissertation Entitled Evolutionary A Dissertation Entitled Evolutionary, Biogeographic, and Population Genetic Patterns of Walleye and other Sander: Relationships across Continents, Corridors, and Spawning Sites by Amanda E. Haponski Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Doctor of Philosophy Degree in Biology (Ecology) _________________________________________ Dr. Carol A. Stepien, Committee Chair _________________________________________ Dr. Timothy G. Fisher, Committee Member _________________________________________ Dr. Johan F. Gottgens, Committee Member _________________________________________ Dr. Patrick M. Kocovsky, Committee Member _________________________________________ Dr. Wendylee Stott, Committee Member _________________________________________ Dr. Patricia R. Komuniecki, Dean College of Graduate Studies The University of Toledo August 2013 Copyright © 2013, Amanda Erin Haponski Chapters 1 and 5 of this document are copyrighted material. Under copyright law, those parts of this document may not be reproduced without the expressed permission of the author. An Abstract of Evolutionary, Biogeographic, and Population Genetic Patterns of Walleye and other Sander: Relationships across Continents, Corridors, and Spawning Sites by Amanda E. Haponski Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Doctor of Philosophy Degree in Biology (Ecology) The University of Toledo August 2013 Understanding a species’ hierarchical genetic variation may provide insights into its ability to cope with current and future stressors, such as climate change, exploitation, and degradation of habitat. Analyzing the events that led to speciation and population diversification may give a framework for predicting responses and adaptations to future changes, imparting critical information for conservation managers. I resolve the evolutionary history and population genetic patterns of the walleye Sander vitreus using molecular and morphological characters and a variety of analyses, including sequences from three nuclear and three mitochondrial (mt) DNA regions and nine nuclear DNA microsatellite (μsat) loci. Results show that walleye and its sister species the sauger S. canadensis diverged ~15.4 Mya (5.2-27.1 Mya = 95% highest posterior density (HPD)), with modern walleye haplotypes differentiating ~10.6 Mya (6.9-14.3 HPD), when climate changes were occurring across North America. Walleye exhibit significant genetic structure (mean FST mtDNA control region=0.24, μsat=0.10) and substantial genetic diversity (mean control region=0.53, μsat=0.68) across its range, at broad- and fine- scales. Contemporary patterns correspond to a genetic isolation by geographic distance iii hypothesis, with northern populations reflecting differential contribution from three distinct Pleistocene glacial refugia. Comparisons of historic versus modern samples from Lake Erie reveal that allelic frequencies have changed over ~70 years (mean FST control region=0.26, μsat=0.17), with modern populations having higher diversity (mean control region=0.67, μsat=0.72 vs. control region=0.05, μsat=0.47). Today’s higher diversity may be due to population rebounds following closure of the walleye fishery in 1970. Paratypes of the historic blue pike did not differ morphologically or genetically from walleye, indicating that the blue pike was not a separate taxon. Additional fine-scale results within the highly degraded Huron-Erie Corridor reveal the seven spawning groups show a mixture of connectivity and divergence. This study also discerns the effects of habitat augmentation on the genetic structure of walleye spawning groups, finding that populations are distinct and have similar levels of genetic diversity (mean control region=0.73, μsat=0.72). Some genetic exchange occurred at an augmentation site, suggesting that walleye from other locations arrived to spawn on the newly available habitat. Such migration could change the genetic composition of the original spawning group. The results of this dissertation provide insight to the processes that shaped the evolution and population genetic patterns of today’s walleye, including past climate change, Pleistocene glaciations, and anthropogenic stressors. Future research identifying the adaptations underlying the genetic diversity and divergence patterns discerned here and their respective genetic contributions to fitness will aid efforts to sustain natural populations in the face of ongoing climate change and other anthropogenic stressors. iv To my husband, family, and friends for all of their love and support “Alive without breath, As cold as death; Never thirsty, ever drinking, All in mail never clinking.” -Gollum, J.R.R. Tolkien’s The Hobbit Acknowledgements This degree was a long worthwhile journey, with numerous people to thank for their help, support, and guidance through it. First and foremost, I am grateful to my advisor, Dr. Carol Stepien, for her support and mentoring throughout the course of my graduate career. Thank you for taking the time to help me grow as a scientist through all of your guidance and encouragement throughout this process. Thanks to the members of my graduate committee, Drs. Timothy Fisher, Johan Gottgens, Patrick Kocovsky, and Wendylee Stott for their valuable input and guidance throughout this journey. To my colleagues in the Great Lakes Genetics/Genomics Laboratory and the Lake Erie Center: Carson, Doug, Jhonatan, Joshua, Lindsey, Matt, Shane, and Tim, thank you for all of your help and being a valuable sounding board. To Matt, thank you for all that you have taught me. I also am very grateful to other members of the Lake Erie Center: Betsy, Jenn, Kristen, Nate, Rachel L., Rachel K., Meredith, Pat (a.k.a. Mom) for their help. I thank my husband, Michael Bagley, for his patience, understanding, and support he has provided me through this degree. I know this was not an easy path for us to take, but it was worth it in the end . To my family, Arthur, Sheila, and Alexis Haponski, for always pushing me to do my best. Last but not least I thank my in-laws David, Mary, Alex, and Chelsea Bagley for all of their support. vi Table of Contents Abstract .............................................................................................................................. iii Acknowledgements ............................................................................................................ vi Table of Contents .............................................................................................................. vii List of Tables .................................................................................................................. xii List of Figures .................................................................................................................. xiv Preface................................................................................................................................xv 1 Introduction………………………………………………………………………..1 2 Phylogenetic and biogeographic relationships of the Sander pikeperches (Perciformes: Percidae): Patterns across North America and Eurasia…………….7 2.1 Abstract… .........................................................................................................7 2.2 Introduction .......................................................................................................8 2.2.1 Morphological differentiation ...........................................................11 2.2.2 Species distributions .........................................................................12 2.2.3 Comparative life histories .................................................................14 2.2.4 Objectives and questions ...................................................................16 2.3 Materials and methods ....................................................................................17 2.3.1 Sampling and DNA extraction ..........................................................17 2.3.2 Gene amplification and DNA sequencing ........................................18 2.3.3 Data analyses ....................................................................................20 vii 2.3.4 Divergence time estimates ................................................................22 2.4 Results…… .....................................................................................................23 2.4.1 Phylogenetic relationships ................................................................23 2.4.2 Biogeographic relationships ..............................................................24 2.4.3 Phylogenetic signal of mitochondrial and nuclear gene regions ......25 2.4.4 Genetic diversity of Sander spp. .......................................................26 2.5 Discussion…… ...............................................................................................27 2.5.1 Evolution and divergence of Sander. ................................................27 2.5.2 Phylogenetic and biogeographic patterns on each continent. ...........31 2.5.3 Phylogenetic signal of gene regions. ................................................33 2.5.4 Genetic diversity patterns. ................................................................37 2.5.5 Conclusions. ......................................................................................41 2.6 Acknowledgements…… .................................................................................42 3 A population genetic window into the
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