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[Pages:220]GENETIC STRUCTURE OF NORTHERN FLYING SQUIRREL (GLAUCOMYS SABRINUS) AND RED SQUIRREL (TAMIASCIURUS HUDSONICUS) POPULATIONS IN THE BLACK HILLS

BY Alyssa M. Kiesow B.S., South Dakota State University, 2000 M.S., South Dakota State University, 2003

A Dissertation Submitted in Partial Fulfillment of The Requirements for the Degree of Doctor of Philosophy College of Arts and Sciences Biological Sciences The University of South Dakota August 2008

Copyright by ALYSSA M. KIESOW

2008 All Rights Reserved

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The members of the Committee appointed to examine the dissertation of Alyssa M. Kiesow find it satisfactory and recommend that it be accepted. __________________________________________ Chairperson, Dr. Hugh Britten __________________________________________ Dr. Lisa Wallace ___________________________________________ Dr. Daniel Soluk ___________________________________________ Dr. Molly Nepokroeff ___________________________________________ Dr. Charles Dieter

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ACKNOWLEDGEMENTS I would like to thank my graduate committee (Dr. Hugh Britten, Dr. Lisa Wallace, Dr. Daniel Soluk, Dr. Molly Nepokroeff, and Dr. Charles Dieter) for their assistance with my project. A special thanks goes to Dr. Hugh Britten (major advisor), for his added efforts with my research and writing, Dr. Lisa Wallace, for her expertise and assistance, and Dr. Charles Dieter, for his guidance and support. The South Dakota Department of Game, Fish and Parks in Pierre, South Dakota provided my research funding through a State Wildlife Grant (Grant Number 2414), which was allocated by the United States Fish and Wildlife Service. The University of South Dakota provided additional financial assistance through matching funds and by providing me with a research fellowship through the University of South Dakota Alumni Foundation in order to conduct my research. Without the research funding and fellowship, my research would have been difficult to conduct. I am thankful for the help provided to me by several individuals. Melissa Hough, a Master of Science graduate, trapped areas of the Black Hills for three years, collecting samples from each squirrel for my genetics research. She is a great researcher and friend. Dr. Mitchell McGaughlin assisted with the numerous microsatellite and DNA sequence "runs" on the infamous ABI Prism sequencer. Mitch Greer and Samuel Cahoy were integral in the collection of samples west of the Black Hills, and Brittany Seiler was important to the collection of samples east of the Black Hills and dissection of red squirrels. All of these individuals put forth much time and effort toward my research, and I am grateful for their assistance.

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A sincere thank you goes out to state and federal biologists and their respective agencies for their assistance in obtaining samples for genetic data analyses. These agencies include Montana Parks and Wildlife Commission, Custer National Forest, Black Hills National Forest, Shoshone National Forest, Payette National Forest, Utah Department of Wildlife, Wyoming Game and Fish Commission, Bighorn National Forest, Medicine Bow National Forest, Kootenai National Forest, Minnesota Department of Natural Resources, and Wisconsin Department of Natural Resources. It was a pleasure working with each individual and their respective agencies.

Finally and most importantly, special thanks go to my husband, Joshua Kiesow; my daughter, Kaylee Kiesow; and my parents, Thomas and Karla Kalis, for inspiring me to reach my goals and supporting me along the way. Without their help, I would not have achieved my goals. My sister and brother-in-law, Joalle and Daniel Holmberg; my nephew, Samuel Holmberg; and my husband's parents, Redgy and Christine Kiesow, receive special thanks for helping me stay strong and positive. Josh, my loving husband and best friend, provided encouragement and comfort during trialing times, and I love and cherish all the moments we have together.

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ABSTRACT

GENETIC STRUCTURE OF NORTHERN FLYING SQUIRREL (GLAUCOMYS SABRINUS) AND RED SQUIRREL (TAMIASCIURUS HUDSONICUS) POPULATIONS IN THE BLACK HILLS

By Alyssa M. Kiesow

May 2008

The Black Hills are unique geological formations with coniferous and prairie vegetation, and are essentially a forested island in a lowland grassland area that is disjunct from surrounding montane areas. We trapped northern flying squirrels (Glaucomys sabrinus) and red squirrels (Tamiasciurus hudsonicus) in the Black Hills from 2005 to 2007 to collect ear samples to elucidate genetic structure of these populations. In addition, we trapped these squirrels in Montana, Wyoming, Idaho, Utah, Minnesota, and Wisconsin to help infer population phylogenies with special consideration of the Black Hills population. Microsatellite loci and mtDNA sequences were used for various genetic data analyses on parentage, genetic structure, and phylogeography. Populations of these squirrels have low observed heterozygosity, i.e., lower than what is expected. In parentage analyses, flying squirrels have 29 true parent pairs of populations sampled at the 80% confidence level with ~0.5 relatedness among pairs. Red squirrels have 60 true parent pairs of populations sampled at the 80% confidence level with ~0.3 relatedness among pairs. In genetic structure analyses, flying squirrels likely have two to three subpopulations in the areas sampled, according to STRUCTURE and GENELAND, but little to no substructure, as indicated by low FST (0.04). Individuals from the northern Black Hills provide more migrants (~4) to the central Black Hills than to other regions, though this is not recent. Red squirrels likely have two to three subpopulations in the areas sampled, according to STRUCTURE and GENELAND, and weak substructure, as indicated by low FST (0.03). The subpopulation in the central Black Hills seems to be isolated from other subpopulations, yet it receives migrants (~4) from the southern Black Hills, though this is not recent. For both squirrels, phylogenies group the Black Hills and Bear Lodge Mountain populations together. Both squirrels are indicated to have two to three subpopulations with weak to no substructure, which suggests that these squirrels have adequate gene flow within the Black Hills. However, phylogenetic trees show the distinctiveness of the Black Hills population, indicating lack of genetic exchange with other nearby mountain ranges. Therefore, the reclassification of subspecific names for both squirrels should be considered.

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TABLE OF CONTENTS ACKNOWLEDGEMENTS........................................................................iv ABSTRACT...........................................................................................vi LIST OF TABLES....................................................................................x LIST OF FIGURES................................................................................xiii CHAPTER 1 ? INTRODUCTION AND STUDY AREA

Introduction....................................................................................1 Study area......................................................................................5 Goals of the Study..........................................................................14 CHAPTER 2 ? CHARACTERIZATION AND ISOLATION OF FIVE ADDITIONAL MICROSATELLITE LOCI IN NORTHERN FLYING SQUIRRELS, GLAUCOMYS SABRINUS (SCIURIDAE, RODENTIA) FOR THE PURPOSES OF THIS RESEARCH Introduction.................................................................................15 Methods......................................................................................15 Results/Discussion.........................................................................18 CHAPTER 3 ? PARENTAGE OF NORTHERN FLYING SQUIRREL (GLAUCOMYS SABRINUS ) POPULATIONS IN THE BLACK HILLS Introduction.................................................................................21 Methods......................................................................................22 Results.......................................................................................27 Discussion...................................................................................33 CHAPTER 4 ? GENETIC STRUCTURE AND LANDSCAPE GENETICS OF NORTHERN FLYING SQUIRRELS (GLAUCOMYS SABRINUS) POPULATIONS FROM THE BLACK HILLS Introduction.................................................................................38 Methods......................................................................................40

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Results.......................................................................................47 Discussion...................................................................................54 CHAPTER 5 ? PHYLOGEOGRAPHY OF THE NORTHERN FLYING SQUIRREL (GLAUCOMYS SABRINUS) POPULATION IN THE ROCKY MOUNTAINS, BLACK HILLS, AND MIDWEST Introduction.................................................................................60 Methods......................................................................................61 Results.......................................................................................69 Discussion...................................................................................82 CHAPTER 6 ? PARENTAGE OF AMERICAN RED SQUIRREL (TAMIASCIURIUS HUDSONICUS) POPULATIONS IN THE BLACK HILLS Introduction.................................................................................89 Methods......................................................................................91 Results.......................................................................................94 Discussion.................................................................................102 CHAPTER 7 ? GENETIC STRUCTURE AND LANDSCAPE GENETICS OF AMERICAN RED SQUIRREL (TAMIASCIURIUS HUDSONICUS) POPULATIONS FROM THE BLACK HILLS Introduction................................................................................106 Methods....................................................................................108 Results......................................................................................115 Discussion.................................................................................122 CHAPTER 8 ? PHYLOGEOGRAPHY OF THE N AMERICAN RED SQUIRREL (TAMIASCIURIUS HUDSONICUS) POPULATION IN THE ROCKY MOUNTAINS, BLACK HILLS, AND MIDWEST Introduction................................................................................129 Methods....................................................................................130

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