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GENE FLOW PATTERNS of the FIVE LINED SKINK EUMECES FASCIATUS in the FRAGMENTED LANDSCAPE of NORTHEAST OHIO a Thesis Presented To

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GENE FLOW PATTERNS OF THE FIVE LINED SKINK EUMECES FASCIATUS IN THE FRAGMENTED LANDSCAPE OF NORTHEAST OHIO A Thesis Presented to The Graduate Faculty of The University of Akron In Partial Fulfillment of the Requirements for the Degree Master of Science Tara Buk May, 2014 GENE FLOW PATTERNS OF THE FIVE LINED SKINK EUMECES FASCIATUS IN THE FRAGMENTED LANDSCAPE OF NORTHEAST OHIO Tara Buk Thesis Approved: Accepted: Advisor Dean of the College Dr. Francisco Moore Dr. Chand K. Midha Faculty Reader Dean of the Graduate School Dr. Randall Mitchell Dr. George R. Newkome Faculty Reader Date Dr. Peter Niewiarowski Department Chair Dr. Monte E. Turner ii ABSTRACT A major obstacle to the preservation of animal populations is habitat fragmentation. Fragmentation often results in the isolation and subsequent loss of subpopulations. Gene flow determines the extent to which populations remain separated as independent evolutionary units, and thus affects the evolution of a species. Gene flow between small fragmented subpopulations can often have great effects on the species stability. If small populations are lost and there is no migration between subpopulations, recolonization of suitable habitat does not occur and the overall population declines. The loss of naturally occurring populations reduces gene flow, which may lead to genetic differentiation. This study investigated the population structure of the five-lined skink, Eumeces fasciatus, occupying what appear to be isolated sites in the fragmented landscape of Northeast Ohio. Populations in Akron were of particular interest because they exist in highly urbanized locales, and these lizards have rarely been recorded in Summit County. Additionally, there is a large gap in distribution record of the species statewide. Five polymorphic microsatellite markers were used to evaluate the gene flow between 5 different locations in Northeast Ohio. The gene flow estimates indicated that there is a significant pattern of isolation by distance (IBD). However, even across very broad geographical scales (170km), the IBD did not lead to a consequential divergence of populations. This data offers information on the genetic divergence of this species and contributes to our understanding of the larger problem of animal conservation in urban areas, as well as its relation to anthropogenic habitat fragmentation and degradation. iii ACKNOWLEDGEMENTS iv TABLE OF CONTENTS Page LIST OF FIGURES vi LIST OF TABLES vii CHAPTER I. INTRODUCTION AND BACKGROUND 1 II. MATERIALS AND METHODS 6 Study system 6 Population sampling 6 Genotyping 8 Statistical analysis 8 III. RESULTS 10 FIT 10 F IS 10 FST 10 Isolation by distance 12 IV. DISCUSSION 18 Regional population structure 18 Local population structure 19 V. CONCLUSIONS 28 REFERENCES 30 v LIST OF FIGURES Figure Page 1 Distribution Map of E.fasciatus populations samples for this study 5 2 The Mantel tests based on pairwise differentiation values indicated a significant pattern of isolation by distance when the two summit county populations were treated as one subpopulation rather than two 15 3 The Mantel tests based on pairwise differentiation values indicated a significant pattern of isolation by distance when the two Summit County populations were treated separately 16 vi LIST OF TABLES Table Page 1 Populations name, county, sample size (N), GPS coordinates, and FIS values. FIS was significantly greater than zero in every population, using a randomization test with 25,000 randomizations for each of the sampled Eumeces fasciatus breeding populations. (P-value for FIS within samples. based on: 25000 randomizations. Indicative adjusted nominal level (5%) for one table is: 0.002) 4 2 Locus name, number of alleles, F , F ,and F values for each IT IS ST locus and over all loci. Bootstrapping was performed over all loci to determine 95% confidence interval. All values are significant p<.05 12 3 Matrix of geographical distances (km) between the populations studied, above the diagonal, and F S values between pairs of E. fasciatus T populations of below the diagonal. All F S values were significantly greater than 0 (p<.005) 200 permutations).T 13 4 Matrix of Nm values between pairs of populations of E. fasciatus below the diagonal. All Nm values were significant (p <.005) 14 vii CHAPTER I INTRODUCTION AND BACKGROUND Population connectivity plays a crucial role in species survivability, particularly in areas affected by habitat degradation and fragmentation. Considering the continual rise in anthropogenic fragmentation, it is not surprising that understanding population connectivity has become primary goal of conservation ecology. In particular, studies that investigate gene flow between subpopulations are needed to determine whether populations are isolated, or part of the connected metapopulation that is capable of recolonization. Previous research indicates that reptiles frequently exist in a matrix of connected subpopulations, or metapopulations (Joyal 2001, Pianka 1996, Sarre 1995, Templeton 2011). Dispersal between subpopulations is needed for the persistence of the regional metapopulation and thus plays a fundamental role in population dynamics. However, directly measuring dispersal of individuals has proven to be fairly difficult and fails to reflect the reproductive success of migrants that determines their influence on a population’s persistence. Measurement of the gene flow between populations is a simpler and more useful way to infer dispersal rates, probability of recolonization, and thus regional connectivity within the metapopulation (Howes 2006). Gene flow is directly relevant to population connectivity because gene flow data can be used to interpret reproductive success of migrants between populations rather than just movement of individuals. 1 Understanding rates of gene flow between fragmented populations can help recognize populations under threat, and clarify the degree to which loss of local populations reduce overall genetic diversity within the taxon. Management of endangered groups therefore needs to treat most populations separately because of their genetic distinctiveness and low rates of genetic exchange (Dubey 2010). Differences in dispersal among subpopulations contribute to genetic differentiation; genetic patterns can then serve as a signal of disruptions in regional population connectivity due to the effect of demographic alterations. Isolated subpopulations may be subject to increased risk of local extinction (Frankham 2005). Landscape-level processes on the population biology of reptiles are critical, especially for species inhabiting anthropogenically modified landscapes (Purrenhage 2009). Many studies have clearly shown that gene flow between populations is often affected by anthropogenic habitat change causing patch isolation. This type of relationship is referred to as Isolation By Distance (IBD). IBD focuses on the genetic effect of geographic isolation among patches, that is to say, it focuses on the general landscape rather than the state of the habitat patches directly. Other factors can combine with IBD to determine the ultimate genetic structure of a population (Hoffman 2004). The focus this study is on urbanization effects rather than glacial advance and retreat as in previous studies. Geologic changes such as glacial advance may alter the population structure of animals but they are a relatively slow process. This study focuses on anthropogenic habitat change that has occurred over a short period of time. A previous study using mtDNA showed that phylogeographic patterns for E. fasciatus were related to divergence that predates the Pleistocene (Howes, 2006). There are no studies on this species that explore the impacts of urbanization in the last century. Little is known about the population dynamics of Eumeces fasciatus in the fragmented landscape of Northeast Ohio. Although the species had not been recorded 2 in Summit County in the last 5 decades, a seemingly robust population of this species has recently been located in the city of Akron. Consequently, this species offers us an opportunity to investigate the current gene flow between populations that may have been isolated due to habitat fragmentation. In order to better understand the viability of the species in this region we must understand the dispersal between subpopulations. Here we run a genetic analysis on five E. fasciatus subpopulations in Northern Ohio using nuclear DNA microsatellite data to determine gene flow. Because gene flow is an indicator of connectivity between subpopulations, it allows us to infer the probability of recolonization. This study helps determine if the Akron populations are connected both within the city and across the region. 3 Table 1: Populations name, county, sample size (N), GPS coordinates, and FIS values. FIS was significantly greater than zero in every population, using a randomization test with 25,000 randomizations for each of the sampled Eumeces fasciatus breeding populations. (P-value for FIS within samples. based on: 25000 randomizations. Indicative adjusted nominal level (5%) for one table is: 0.002) 4 Figure 1: Distribution Map of E. fasciatus populations samples for this study 5 CHAPTER II MATERIALS AND METHODS Study system Five-lined skinks are small to medium size lizards growing to about 12.5 cm to 21.5 cm total in length. Young five-lined Skinks are dark brown to black with five distinctive white to yellow stripes running along the body and a bright blue tail. In females, the blue color fades to a light blue with age, and
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