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Evolutionary Dynamics Among Salamanders in the Plethodon Glutinosus Group, with an Emphasis on Three Species: P

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Evolutionary Dynamics Among Salamanders in the Plethodon Glutinosus Group, with an Emphasis on Three Species: P Evolutionary dynamics among salamanders in the Plethodon glutinosus group, with an emphasis on three species: P. jordani, P. metcalfi, and P. teyahalee (Caudata: Plethodontidae) by Matthew Williams Howard Chatfield A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) In The University of Michigan 2009 Doctoral Committee: Professor Priscilla K. Tucker, Co-Chair Professor Ronald A. Nussbaum, Co-Chair Professor, Jeffrey C. Long Assistant Professor Thomas F. Duda, Jr Copyright Matthew Williams Howard Chatfield 2009 ACKNOWLEDGEMENTS This dissertation would not have been possible without the help and guidance of a great many people and institutions. I would especially like to thank Priscilla Tucker for her patience and willingness to engage at every stage of this long process. Her dedication, not just to research, but education as well has made this project possible. I would also like to thank my other committee members: Ron Nussbaum, Tom Duda, and Jeff Long. A few people have provided early insight into the study system, most notable are Richard Highton and Stephen Tilley. These acknowledgements would not be complete without mentioning Nelson Hairston, Sr. Although I only the chance to meet him once before his death last summer, his work on plethodontid biology and this study system in particular laid the groundwork for this dissertation. The work presented here is the product of a long and expensive endeavor, and there are many institutions that have generously given their financial support. Many departments and institutions within the University of Michigan have been especially generous, including the Department of Ecology and Evolutionary Biology, the Museum of Zoology, Rackham Graduate School, and the Department of Human Genetics. Other essential granting institutions and societies include: the National Institutes of Health, the Society for the Study of Amphibians and Reptiles, and the North Carolina Herpetological Society. ii Lab work was undoubtedly the largest component of this project, and the learning curve was steep. For their help, I would like to thank past and present members of the Tucker Lab, especially Les Harris for showing me the ropes of lab work. Elizabeth Jockusch gave me much needed nuclear DNA primers, and time and patience after that. David Weisrock provided help with the mtDNA primers, and his own dissertation work on the Plethodon jordani complex is often cited in this dissertation. I would also like to thank Ken Luzynski and Armand Conti for spending last summer genotyping samples in the lab. Field work was not only an essential component of my dissertation work, but provided a much needed respite from urban life. For making work in the Smokies and my summers in the field an absolute pleasure, I would like to thank the crew at the Appalachian Highlands Science Learning Center at Purchase Knob, especially Paul Super, Susan Sachs, Jonathan Mays, and Gabrielle Riesner. Kevin Hamed’s help in the field is almost as appreciated as his wit and humor. I am indebted to Ben Fitzpatrick for his help with the statistical analysis in Chapter III and Ken Kozak for creating the niche models used in Chapter III and IV. Both of these excellent researchers are rightfully co-authors. I would also like to thank Amanda Zellmer for her time and patience in helping with the niche modeling (and other projects not related to this dissertation). For making my graduate career proceed relatively smoothly, I need to thank the staff of the Department of Ecology and Evolutionary Biology, especially LaDonna Walker, Julia Eussen, and Jane Sullivan. I also need to thank the staff at the Museum of iii Zoology, especially Bev Dole, Norah Daugherty, and Robbin Murrell. Their aid in the day-to-day logistics of carrying out this project was invaluable. I am not able to express my gratitude deeply enough to the following people: Lucía Luna for making office life not only tolerable, but fun; Matt Vance for his patience throughout; and Clay Vance for reminding me that it is the love of the organism that ultimately matters. I cannot end these acknowledgements without thanking my parents, Virginia and Robert Chatfield, for instilling the idea that one should always put education and the pursuit of one’s interests above all else. iv TABLE OF CONTENTS ACKNOWLEDGEMENTS ii LIST OF FIGURES vii LIST OF TABLES ix LIST OF APPENDICES x ABSTRACT xi CHAPTER I. Introduction 1 Literature Cited 8 II. Difficulties with species delimitation and DNA barcoding in 14 the Plethodon glutinosus group (Caudata: Plethodontidae) Abstract 14 Introduction 15 Difficulties with species delimitation 18 The Plethodon glutinosus group 26 Taxonomic history of the Plethodon glutinosus group 28 Species delimitation in the Plethodon glutinosus group 30 Conclusion 41 Literature Cited 51 III. Differential introgression of mtDNA relative to nuclear DNA 61 v and morphology in a salamander hybrid zone involving three species (Plethodontidae: Plethodon) Abstract 61 Introduction 62 Methods 65 Results 74 Discussion 78 Literature Cited 124 IV. Past, present, and future range dynamics of the montane 131 salamanders Plethodon jordani and P. metcalfi (Caudata: Plethodontidae) Abstract 131 Introduction 131 Methods 136 Results 138 Discussion 140 Literature Cited 157 V. Conclusion 163 Literature Cited 166 vi LIST OF FIGURES FIGURE 2.1 Competing phylogenetic trees from Palmer et al. (2005) constructed 44 using allozymes and Wiens et al. (2006) constructed using mitochondrial and nuclear DNA 3.1 Map of study area showing collection localities of parental 86 (Plethodon jordani, P. metcalfi, and P. teyahalee) and hybrid samples 3.2 Map of the mtDNA ND2 gene with adjacent tRNA genes and partial 88 map of nuclear ILF3 gene showing relative positions of the middle exon and two introns 3.3 Map of Balsam Mountain showing transect, collection localities, 90 sample sizes, marker scores, and habitat suitability values 3.4 Map of Hyatt Ridge showing transect, collection localities, sample 92 sizes, and marker scores 3.5 Map of Palmer Creek showing transect, collection localities, sample 94 sizes, and marker scores 3.6 Map of Mt Sterling showing transect, collection localities, sample 96 sizes, and marker scores 3.7 Ecological niche modeling results showing present-day predicted 98 geographic distributions for P. jordani and P. metcalfi vii 4.1 Topographical relief map of southern Appalachians highlighting 146 mountain ranges mentioned in text and ecological niche modeling results showing present-day predicted geographic distribution for Plethodon jordani and P. metcalfi 4.2 Ecological niche modeling result showing predicted geographic 150 distribution for Plethodon jordani and P. metcalfi during the last glacial maximum 21,000 years ago 4.3 Ecological niche modeling result showing predicted geographic 153 distribution for Plethodon jordani and P. metcalfi in the year 2050 viii LIST OF TABLES TABLE 2.1 Species currently recognized in the Plethodon glutinosus complex 46 2.2 Taxonomic timeline of the Plethodon glutinosus group 47 2.3 Phases of species delimitation in the Plethodon glutinosus group 50 3.1 Climatic variables used in creation of ecological niche models 101 3.2 Summary of salamander samples from the hybrid zone 102 3.3 Contingency table showing individual sample data used to test for 103 differential patterns of introgression 3.4 Contingency table showing sample localities classified by their 104 most common haplotype 3.5 Results of general linear models (GLMs) 105 3.6 Home range sizes in for males and females of Plethodon 106 jordani, P. teyahalee, and P. metcalfi 4.1 Climatic variables used in creation of ecological niche models 156 ix LIST OF APPENDICES APPENDIX 3.1 Collection localities, sites codes, elevation, and latitude and 107 longitude for animals captured in the hybrid zones 3.2 Collection localities, sites codes, elevation, and latitude and 109 longitude for parental taxa 3.3 Pure parental individuals and marker scores used in panel for 110 marker development 3.4 Samples and marker scores for all samples used in analyses 112 x ABSTRACT Evolutionary dynamics among salamanders in the Plethodon glutinosus group, with an emphasis on three species: P. jordani, P. metcalfi, and P. teyahalee (Caudata: Plethodontidae) by Matthew Williams Howard Chatfield Co-Chairs: Priscilla K. Tucker and Ronald A. Nussbaum This dissertation includes three studies that focus on the evolution of salamanders in the Plethodon glutinosus group (family Plethodontidae), that are found throughout much of the eastern United States. The first study explores species delimitation in taxonomically problematic groups and then, in that context, examines the long and contentious taxonomic history of the P. glutinosus group. Four commonly encountered problems are reviewed: (1) the presence of cryptic species complexes, (2) incomplete lineage sorting, (3) introgressive hybridization, and (4) the application of different species concepts. The history of species description in the P. glutinosus group is then discussed in light of these problems. The controversial use of DNA barcoding is also discussed, as is its potential utility in the group. The second study is a spatially fine-scale analysis of a hybrid zone that occurs among three species within the P. glutinosus group – P. jordani, P. metcalfi, and P. teyahalee – in the southern Appalachian Mountains. Spatial patterns of variation along four transects are examined at four markers: single xi nucleotide polymorphisms located in the mtDNA ND2 gene and the nuclear DNA ILF3 gene and the morphological markers of red cheek pigmentation and white flecks. Concordance among nuclear DNA and both morphological markers across the four transects is observed. In three of the four transects, however, the pattern of mtDNA is discordant from all other markers. This finding, in addition to previous studies demonstrating mating asymmetry and differing ecological niches, suggests the hybrid zone may be moving. The third study uses ecological niche modeling to explore range dynamics of P. jordani and P.
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