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Hemidactylium Scutatum): out of Appalachia and Into the Glacial Aftermath RANGE-WIDE PHYLOGEOGRAPHY OF THE FOUR-TOED SALAMANDER (HEMIDACTYLIUM SCUTATUM): OUT OF APPALACHIA AND INTO THE GLACIAL AFTERMATH Timothy A. Herman A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE August 2009 Committee: Juan Bouzat, Advisor Christopher Phillips Karen Root ii ABSTRACT Juan Bouzat, Advisor Due to its limited vagility, deep ancestry, and broad distribution, the four-toed salamander (Hemidactylium scutatum) is well suited to track biogeographic patterns across eastern North America. The range of the monotypic genus Hemidactylium is highly disjunct in its southern and western portions, and even within contiguous portions is highly localized around pockets of preferred nesting habitat. Over 330 Hemidactylium genetic samples from 79 field locations were collected and analyzed via mtDNA sequencing of the cytochrome oxidase 1 gene (co1). Phylogenetic analyses showed deep divergences at this marker (>10% between some haplotypes) and strong support for regional monophyletic clades with minimal overlap. Patterns of haplotype distribution suggest major river drainages, both ancient and modern, as boundaries to dispersal. Two distinct allopatric clades account for all sampling sites within glaciated areas of North America yet show differing patterns of recolonization. High levels of haplotype diversity were detected in the southern Appalachians, with several members of widely ranging clades represented in the region as well as other unique, endemic, and highly divergent lineages. Bayesian divergence time analyses estimated the common ancestor of all living Hemidactylium included in the study at roughly 8 million years ago, with the most basal splits in the species confined to the Blue Ridge Mountains. This pattern of radiation from the southern Appalachians parallels that of the “Out of Appalachia” hypothesis of the geographic origin of the lungless salamanders, and lends further support to the importance of this region as a generator of biodiversity in eastern North America. iii Female four-toed salamander (Hemidactylium scutatum) attending eggs in Sphagnum moss, Walton County, Florida. iv ACKNOWLEDGMENTS First and foremost I would like to thank my wife, Maria Herman, for the many long hours she spent driving through the night and hunched over moss, as well as her seemingly interminable patience, which allowed me to accomplish this daunting project. I would also like to thank Jeremy Ross for his generous contributions towards driving, collecting samples, and assistance in the laboratory. I thank J. Corser and K. Enge for providing assistance in the field, tissue samples, and collecting localities. I thank R. Bonett, Z. Felix, J. Gilhen, and G. Lipps for providing tissue samples for analysis and help with collecting locations. I thank many who helped with sample collection in the field: K. Bekker, B. Bogaczyk, J. Boundy, C. Carpenter, R. Chalmers, B. Gasdorf, I. Guenther, K. Hamed, T. Majure, K. McGrath, P. Moler, J. Petranka, C. Phillips, B. Roller, V. Schneider, J. Settles, K. Stanford, E. Timpe, and L. Williams. I also thank many more who assisted with identifying collecting localities: R. Altig, S. Bennett, A. Braswell, A. Breisch, J. Briggler, C. Brune, C. Camp, M. Eliott, J. Gardner, W. Gibbons, J. Gillingham, S. Graham, C. Guyer, C. Hall, S. Hall, J. Harrison, A. Hebda, D. Hipes, J. Hohman, K. Irwin, J. Jensen, T. Johnson, R. Jones, S. Kilpatrick, T. Mann, J. MacGregor, R. Montanucci, K. Morris, T. Pauley, R. Pfingsten, S. Roble, A. Sanders, M. Sasser, D. Saugey, D. Stevenson, M. Sisson, J. Skeen, J. Taylor, S. Trauth, T. Walsh, and C. Wilson. I thank my father, Michael Herman, for assisting with a portion of travel, and the Toledo Naturalists’ Association for partial funding of labwork through the Harold F. Mayfield Grant. I thank my committee members and R. Bonett for helpful comments on the manuscript. Finally I thank the Toledo Zoo for professional development funding and R. Andrew Odum and the rest of the zoo’s Department of Herpetology for accommodating my many collecting trips. v TABLE OF CONTENTS Page INTRODUCTION ................................................................................................................. 1 METHODS ............................................................................................................ 6 Sampling ............................................................................................................ 6 DNA Extraction, Amplification, and Sequencing ..................................................... 7 Phylogeographic Analysis ......................................................................................... 8 RESULTS ............................................................................................................ 14 Sequence Variation .................................................................................................... 14 Genetic Structure and Patterns of Distribution .......................................................... 14 Mismatch Distributions and Tests of Recent Expansion ........................................... 22 Mantel Tests of Barriers............................................................................................. 24 Divergence Time Estimates ....................................................................................... 25 DISCUSSION ............................................................................................................ 27 Conservation Implications ......................................................................................... 38 Conclusions ............................................................................................................ 39 REFERENCES ...................................................................................................................... 42 APPENDICES ....…………………………………………………………………… 49 1 Number of samples and haplotypes/clades detected at each collecting locality included in the study ....................................................................... 50 2 Results of Tajima’s D and Fu’s Fs tests......................................................... 52 3 Haplotype networks of individual clades ....................................................... 53 4 Topographic relief map of the southern Appalachian Mountains, vi showing major physiographic features and proposed hydrological barriers to dispersal discussed in the text ...................................................... 56 5 Review of co-distributed taxa with phylogeographic patterns concordant with those resolved in Hemidactylium ....................................... 57 LIST OF FIGURES Figure Page 1 Documented range of Hemidactylium scutatum, showing the 79 sampling locations included in this study. ................................................................................. 5 2 Bayesian 50% majority rule consensus phylogram generated from 77 unique ingroup co1 haplotype sequences and 2 outgroup sequences. ................................... 15 3 Map of geographic distribution of major clades and subclades as defined by phylogenetic analyses. ............................................................................................... 17 4 Haplotype networks generated by TCS overlaid on the distribution of Hemidactylium scutatum ........................................................................................... 21 5 Observed pairwise mismatch distributions for all samples together, and for Clades A through E .................................................................................................... 23 6 Generalized map of phylogeographic patterns of expansion resolved in Hemidactylium scutatum. ........................................................................................... 28 vii LIST OF TABLES Table Page 1 Distribution of haplotype and nucleotide diversity and haplotypes among clades and number of sites and samples where representatives from each clade were detected ................................................................................... 16 2 Mean uncorrected genetic distance [SE] -- between clades (below diagonal), and within clades (on diagonal, in boldface type). ................................................... 18 3 Results of partial Mantel tests of hypothesized geographic barriers to dispersal ............................................................................................................ 24 4 Divergence time estimates for selected clades and subclades generated by the Bayesian coalescent approach in BEAST ............................................................ 26 1 INTRODUCTION The forests, mountains, and waterways of eastern North America are renowned for their biodiversity. Many taxa have undergone extensive radiations in this region that occur nowhere else on earth, such as radiations of over 330 crayfish species in the family Cambaridae (Crandall and Buhay 2008), nearly 200 darter species in the subfamily Etheostomatinae (FishBase 2009; Jelks et al. 2008), and 293 mussel species in the order Unionoida (MUSSEL Project 2009). Similarly, eastern North America is the global center of diversity for living salamanders (order Caudata), with 7 of the 10 living families represented in the region. Of these, the Plethodontidae (Lungless salamanders) is the most diverse, currently containing 383 (67%) of the world’s described caudates. Since Wilder and Dunn first published
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