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MIAMI UNIVERSITY The Graduate School Certificate for Approving the Dissertation We hereby approve the Dissertation of Zachary St. John Taylor Candidate for the Degree: Doctor of Philosophy _____________________________________ Susan M.G. Hoffman, Director _____________________________________ David J. Berg, Reader _____________________________________ Brian Keane, Reader _____________________________________ Douglas B. Meikle _____________________________________ Emily S. Murphree Graduate School Representative ABSTRACT GEOGRAPHICAL HETEROGENEITY AND LANDSCAPE-SCALE GENETIC PATTERNS IN GREAT LAKES POPULATIONS OF PEROMYSCUS Zachary S. Taylor Woodland mice of the genus Peromyscus are broadly distributed throughout North America, where they interact with a wide variety of landscape features, climates, and biological communities. Each of the central chapters of this dissertation examines genetic heterogeneity in a species of Peromyscus in relation to landscape features of the Great Lakes region, in order to illuminate the biogeographical constraints facing small mammals in this region. Chapter 1, General introduction Chapter 2, MtDNA genetic structure transcends natural boundaries in Great Lakes populations of deer mice (Peromyscus maniculatus gracilis), examines the genetic structure of deer mice to describe the effect of the Great Lakes on the colonization of northern Michigan from southern refugial sources after the end of the last glacial cycle. Analyses reveal a complex structure indicating occasional migration across Lake Michigan during the 10,000-year history of mouse habitation in the region. Chapter 3, Landscape fragmentation and geographical isolation define microsatellite genetic structure in Great Lakes populations of deer mice (Peromyscus maniculatus gracilis), describes the genetic structure of deer mice using nuclear microsatellite markers. In contrast to Chapter 2, which examines the Great Lakes as barriers to postglacial colonization, Chapter 3 considers the role of the lakes in promoting the differentiation of populations through genetic drift, after expansion from a common source. Chapter 4, Landscape-scale fragmentation and genetic structure in populations of the northern white-footed mouse (Peromyscus leucopus noveboracensis), describes the genetic structure of white-footed mice along a transect from southern Ohio to northern Michigan. Because this transect covers a heterogeneous landscape and climatic gradient, habitat fragmentation and biogeographical range limitation are considered as possible determinants of genetic patterns. Chapter 5, Conclusion GEOGRAPHICAL HETEROGENEITY AND LANDSCAPE-SCALE GENETIC PATTERNS IN GREAT LAKES POPULATIONS OF PEROMYSCUS A DISSERTATION Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Zoology by Zachary S. Taylor Miami University Oxford, Ohio 2010 Dissertation Director: Susan M.G. Hoffman © Zachary S. Taylor 2010 Table of Contents List of Tables ................................................................................................................. iv List of Figures ................................................................................................................. v CHAPTER 1 General Introduction .............................................................................. 1 Overview ......................................................................................................................... 1 Background ..................................................................................................................... 2 References ....................................................................................................................... 8 CHAPTER 2 MtDNA genetic structure transcends natural boundaries in Great Lakes populations of deer mice (Peromyscus maniculatus gracilis) ........................... 12 Introduction ................................................................................................................... 13 Materials and methods .................................................................................................. 15 Results ........................................................................................................................... 21 Discussion ..................................................................................................................... 23 Acknowledgements ....................................................................................................... 27 References ..................................................................................................................... 28 For 2 groups, with eastern populations only ............................................................. 35 CHAPTER 3 Natural landscape fragmentation defines microsatellite genetic structure in Great Lakes populations of deer mice (Peromyscus maniculatus gracilis) ........................................................................................................................................... 42 CHAPTER 4 Landscape-scale fragmentation and genetic structure in populations of the northern white-footed mouse (Peromyscus leucopus noveboracensis) ............. 68 Abstract ......................................................................................................................... 68 Introduction ................................................................................................................... 69 Materials and Methods .................................................................................................. 71 Results ........................................................................................................................... 74 Discussion ..................................................................................................................... 76 Acknowledgments ........................................................................................................ 79 References ..................................................................................................................... 80 CHAPTER 5. Conclusion .............................................................................................. 95 References ................................................................................................................... 101 iii List of Tables Chapter 2 Table 1. Differentiation of populations and population divisions in Great Lakes Peromyscus maniculatus 33 Table 2. Differentiation of populations and population divisions in Great Lakes Peromyscus maniculatus 34 Chapter 3 Table 1. Microsatellite loci selected for analysis 61 Table 2. Molecular diversity indexes for populations of Peromyscus maniculatus 62 Chapter 4 Table 1. Microsatellite loci selected for analysis 85 Table 2. Standard molecular diversity indexes for populations of Peromyscus leucopus 86 iv List of Figures Chapter 2 Figure 1. Distribution of Peromyscus maniculatus gracilis haplogroups in the central Great Lakes region 35 Figure 2. Bayesian haplotype tree for Great Lakes Peromyscus maniculatus gracilis and related groups 36 Figure 3. Parsimony network for Great Lakes and North Carolina Peromyscus maniculatus 37 Mismatch analysis of Peromyscus maniculatus samples 38 Chapter 3 Figure 1. Trapping locations for Peromyscus maniculatus gracilis in the Great Lakes region 63 Figure 2. Spatial distribution of genetic structure for Peromyscus maniculatus gracilis 64 Figure 3. Clustering of Michigan populations of Peromyscus maniculatus gracilis by STRUCTURE 65 Chapter 4 Figure 1. Study area and trapping sites for Peromyscus leucopus 87 Figure 2. Habitat availability and genetic diversity for Peromyscus leucopus 88 Figure 3. Inter-population differentiation populations of Peromyscus leucopus 89 Figure 4. Clustering analyses using STRUCTURE 90 v Dedication To Victoria, Stella, June, and my parents, for your endless patience and support. vi Acknowledgements I am indebted to my advisor, Susan Hoffman, for the opportunity to find my way through these exciting projects; and to David Berg, Brian Keane, Douglas Meikle, and Emily Murphree, for their help and patience. I could not have completed this dissertation without assistance from a large number of individuals and institutions, including Phil Myers, Rosa Moscarella, and Robbyn Abbitt, for extraordinary assistance vital to this dissertation. Many students and colleagues have contributed labor to the projects described herein, including Molly Steinwald, Cameron Beech, Justin Campbell, Brett Chatman, Darcy Dayhoff, Brian Dinh, Allison Dixon, and Kyle Westhafer. The staffs of Pigeon River State Forest, Seney National Wildlife Refuge, the Michigan State University Museum, and the University of Michigan Museum of Zoology were instrumental in sampling efforts over the years. Chris Wood, Xiaoyun Deng, and John Hawes of the Center for Bioinformatics and Functional Genomics at Miami University were always extremely knowledgeable and helpful with sequencing and genotyping. This work was completed with funding from the Department of Zoology and the Graduate School at Miami University, and from a Grant-in-Aid provided by the American Society of Mammalogists. vii CHAPTER 1 General Introduction Overview When natural or artificial barriers prevent animals from moving from one area to another, this interference can reduce the chances for long-term survival of affected populations or even species. In extreme