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A Thesis Entitled Molecular, Morphological, and Biogeographic Resolution of Cryptic Taxa in the Greenside Darter Etheostoma Blen

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A Thesis Entitled Molecular, Morphological, and Biogeographic Resolution of Cryptic Taxa in the Greenside Darter Etheostoma Blen A Thesis Entitled Molecular, morphological, and biogeographic resolution of cryptic taxa in the Greenside Darter Etheostoma blennioides complex By Amanda E. Haponski Submitted as partial fulfillment of the requirements for The Master of Science Degree in Biology (Ecology-track) ____________________________ Advisor: Dr. Carol A. Stepien ____________________________ Committee Member: Dr. Timothy G. Fisher ____________________________ Committee Member: Dr. Johan F. Gottgens ____________________________ College of Graduate Studies The University of Toledo December 2007 Copyright © 2007 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 Molecular, morphological, and biogeographic resolution of cryptic taxa in the Greenside Darter Etheostoma blennioides complex Amanda E. Haponski Submitted as partial fulfillment of the requirements for The Master of Science Degree in Biology (Ecology-track) The University of Toledo December 2007 DNA sequencing has led to the resolution of many cryptic taxa, which are especially prevalent in the North American darter fishes (Family Percidae). The Greenside Darter Etheostoma blennioides commonly occurs in the lower Great Lakes region, where two putative subspecies, the eastern “Allegheny” type E. b. blennioides and the western “Prairie” type E. b. pholidotum , overlap. The objective of this study was to test the systematic identity and genetic divergence distinguishing the two subspecies in areas of sympatry and allopatry in comparison to other subspecies and close relatives. DNA sequences from the mtDNA cytochrome b gene and control region and the nuclear S7 intron 1 comprising a total of 1,497 bp were compared from 294 individuals across 18 locations, including the Lake Erie basin and the Allegheny, Meramec, Obey, Ohio, Rockcastle, Susquehanna, and Wabash River systems. Results showed pronounced divergences among taxa ( θST = 0.92 – 0.97; p-distance = 0.025 – 0.039) presently designated as E. b. blennioides , E. b. newmanii , and E. b. pholidotum, as well as identification of a fourth clade in the Meramec River . Most traditional morphological iii characters were significantly different ( P= 0.0001) in distinguishing between E. b. blennioides and E. b. pholidotum , including scale counts and degree of ventral squamation. However, the range of variation within these characters overlapped, obscuring accurate assignment of individuals to the taxa. The four significantly divergent taxa of the Greenside Darter complex should be evaluated further for potential elevation to species status. iv Acknowledgments I am grateful to my advisor, Dr. Carol Stepien, for her support and mentoring throughout the course of my project. I also thank the University of Toledo’s Lake Erie Center and Department of Environmental Sciences for support. This research was funded by grants to C. Stepien from Ohio Sea Grant #R/LR-9PD, USEPA #CR- 83281401-0, and an NSF Research Experience for Undergraduates award #DBI-0243878 (with B. Michael Walton, which sponsored me at the project’s origin during summer 2004). I also thank Douglas Carlson, Todd Crail, Joseph Faber, Jeff Grabarkiewicz, David Neely, and William Zawiski for collection help. Collections were made under scientific collection permits from the states of Michigan and Ohio. Members of the Great Lakes Genetics Laboratory (GLGL), including Joshua Brown, Douglas Murphy, Matthew Neilson, Rex Strange, and Osvaldo Jhonatan Sepulveda Villet helped with field and laboratory work, and provided a valuable sounding board for ideas and improvements. My committee members Dr. Timothy Fisher and Dr. Johan Gottgens made suggestions that improved both the thesis and manuscript, and Dr. Timothy Fisher helped to determine the distribution of the Greenside Darter during the Pleistocene glaciations. Additional aid was provided by Dr. Peter Berendzen with glacial distribution figures, Dr. Brooks Burr with morphological determination, Dr. David Krantz with Quaternary geological information, Dr. Ann Krause with statistical analyses, and Dr. Brady Porter supplied outgroup samples. Patricia Uzmann provided logistic support. I thank my husband, Michael Bagley, for all of the support he has provided me for the past two years and 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, and Alex Bagley for all of their support. v Table of Contents Abstract iii Acknowledgments v Table of Contents vi List of Tables vii List of Figures viii I. Introduction 1 II. Methods 7 III. Results 14 IV. Discussion 21 V. References 35 VI. Tables 48 VII. Figures 54 VIII. Appendices 65 vi List of Tables Table 1. Summary of sampling sites, genetic identity, and statistical 48 comparisons among the Greenside Darter complex taxa. Table 2. Pairwise genetic divergences among taxa comprising the 49 Greenside Darter complex using θST and uncorrected p-distances. Table 3. θST and exact tests of differentiation comparisons for populations 50 of (a) Etheostoma blennioides blennioides and (b) E. b. pholidotum. Table 4. Nested clade analysis results for Etheostoma blennioides 51 blennioides and E. b. pholidotum . Table 5. Morphological characters, counts, and statistical comparisons 52 for Etheostoma blennioides blennioides and E. b. pholidotum . Table 6. Uncorrected p-distances for selected darter sister species based on 53 cytochrome b sequences. vii List of Figures Figure 1. Map showing geographic distribution and sampling sites 54 for taxa comprising the Greenside Darter complex. Figure 2. Morphological characters distinguishing taxa belonging to the 55 Greenside Darter complex, including; (a) scale counts, (b) dorsal lip tip presence and (c) dorsal lip tip absence, (d) complete ventral squamation and (e) incomplete ventral squamation. Figure 3. Phylogenetic trees describing relationships among taxa comprising 56 the Greenside Darter complex based on; (a) mtDNA cytochrome b, (b) mtDNA control region, (c) nuclear DNA S7 intron 1, and (d) combined mitochondrial (both mtDNA cytochrome b and control region). Figure 4. Distribution and frequency of mtDNA cytochrome b haplotypes 61 for (a) Etheostoma blennioides blennioides and (b) E. b. pholidotum. Figure 5. Phylogeographic network analyses showing haplotype relationships 62 for (a) Etheostoma blennioides blennioides and (b) E. b. pholidotum. Figure 6. Hypothetical distribution based on genetic results for the Greenside 63 Darter complex over time for (a) widely distributed ancestor, (b) divergence of Etheostoma blennioides blennioides (~1.8 mya), (c) divergence of E. b. pholidotum , E. b. newmanii , and the Meramec River clade (~1.3 mya), and (d) post-glacial dispersal of E. b. blennioides and E. b. pholidotum. viii Chapter One Introduction Resolution of correct systematic relationships is essential to evolutionary, biogeographic, and ecological studies, enabling us to identify taxa, evaluate divergence patterns among them, and compare diversity across their range. However, the presence of cryptic taxa has confounded many traditional studies since they may appear morphologically similar yet be phylogenetically distinct. Advances in obtaining and analyzing DNA sequences now facilitate delineation of cryptic species and aid in evaluating their component genetic and ecological diversity. Approaches that combine data sets, such as mitochondrial and nuclear DNA sequences and evaluation of traditional morphological characters, are especially powerful for resolving systematic and biogeographic questions among cryptic species groups. The darters (Percidae: Etheostomatinae) are one of the most diverse groups of North American freshwater fishes, comprising more than 200 species (Nelson, 2006). They have undergone remarkable taxonomic diversification, adaptive radiation, and differentiation. This group includes some of the most imperiled endemic freshwater taxa with 40 species listed on the 2006 International Union for the Conservation of Nature and Natural Resources’ Red List of Threatened Species (IUCN, 2006). Species descriptions for the darters traditionally were based upon morphometrics, meristic characters, and male coloration patterns (Page, 1983) that often broadly overlap among taxa. During the 1 1800s, nearly 100 species of darters were described based on morphological characters (Collette, 1967) and were then reorganized into three genera ( Percina , Ammocrypta , and Etheostoma ; Bailey et al., 1954). The genus Etheostoma includes many newly identified cryptic taxa among an estimated 140 species today (Nelson, 2006), many of which were distinguished using DNA sequencing (e.g., Burr and Page, 1993; Porter et al., 2002; Page et al., 2003; Mayden et al., 2005). Rafinesque (1819) originally described the Greenside Darter Etheostoma blennioides , whose name means “blenny-like”, referring to its cryptic color patterns, adhesive eggs in algal nests, and body form superficially similar to members of the Family Blenniidae. The Greenside Darter inhabits lake shores and the rocky riffles of creeks and rivers (Page and Burr, 1991), ranging from the lower Missouri and Ouachita River systems north through the Ohio River basin and the Great Lakes (Fig. 1; Boschung and Mayden, 2004). Rafinesque (1819) designated the type locality of the Greenside Darter as the falls of the Ohio River below Louisville, KY (Lee et al., 1980) that were destroyed when the McAlpine Locks and dam were built in 1975 (Army
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