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Mitochondrial DNA and Y-Chromosome Variation of Eastern Aleut Populations: Implications for the Genetic Structure and Peopling of the Aleutian Archipelago

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Mitochondrial DNA and Y-Chromosome Variation of Eastern Aleut Populations: Implications for the Genetic Structure and Peopling of the Aleutian Archipelago By Mark Zlojutro M.A., University of Kansas, 2006 Copyright 2008 Submitted to the Department of Anthropology and the Faculty of the Graduate School of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy Dr. Michael H. Crawford (Chairperson) Dr. James H. Mielke Committee members Dr. Felix Moos Dr. Rolfe D. Mandel Dr. Stephen H. Benedict Date defended: September 10 th , 2008 i The Dissertation Committee for Mark Zlojutro certifies that this is the approved version of the following dissertation: Mitochondrial DNA and Y-Chromosome Variation of Eastern Aleut Populations: Implications for the Genetic Structure and Peopling of the Aleutian Archipelago Committee: Dr. Michael H. Crawford (Chairperson) Dr. James H. Mielke Dr. Felix Moos Dr. Rolfe D. Mandel Dr. Stephen H. Benedict Date approved: September 16 th, 2008 ii Abstract The Aleuts are the native inhabitants of the Aleutian archipelago off the southwest coast of Alaska and, since Russian contact in 1741, have experienced a series of demographic transitions. This study investigates the impact of historical events on the genetic structure of the Aleut population through analysis of mitochondrial and Y-chromosome DNA variation in five eastern Aleut communities in relation to previous molecular research conducted on communities located further to the west. Results from HVS-I sequencing and Y-SNP and Y-STR typing reveal patterns of variability that exhibit geographic differentiation in an east-west manner. Mitochondrial haplogroups A and D represent the two major maternal lineages observed in the Aleut samples, with haplogroup D more prevalent in the Pribilofs and island groups located to the west. This distribution pattern is likely the result of founder effect related to the forced population resettlements organized by Russian fur traders in the late 18 th and early 19 th centuries. In the eastern Aleutian Islands and lower Alaska Peninsula, higher frequencies of haplogroup A and its subclades were observed and based on archaeological and phylogeographic evidence may represent the genetic signature of sustained cultural and demic exchange with neighboring Eskimo and Na-Dene groups. The relationship between geography and mtDNA variation is further evident from the highly significant correlation of geographic and genetic distance matrices ( r = 0.717) and the decreasing correlogram of spatial autocorrelation values that present a clinal pattern to mtDNA structure. For the Aleut Y-chromosomes, the vast majority were characterized to European haplogroups (approximately 85%), which contrasts the mtDNA picture that reveals only 6.1% non-native matrilines in the eastern region and thus indicating asymmetrical gene flow between European men and Aleut women. Russian paternal lineages are common in the western islands, whereas the predominantly Scandinavian patriline I1a is observed at elevated frequencies in the eastern communities, a consequence of the American purchase of Alaska and the subsequent influx of Scandinavian and US European fishermen into the region. The application of Monmonier’s algorithm and genetic surface interpolations for both genetic systems reveal geographic zones of discontinuity at Umnak and Akutan Islands, underscoring the east-west substructure for the Aleut population. Lastly, phylogeographic analysis of mtDNA data and the results of recent ancient DNA studies suggest that subhaplogroup D2 evolved in Beringia and may represent the ancestral gene pool for both Paleo-Eskimos and Aleuts. Overall, this study identifies a significant relationship between geography and genetic variation in the Aleut population, with a distinct substructure along an east-west axis. These regional differences are due to a combination of historical founder effects, male-biased gene flow from European populations, and the peopling of the Aleutian Archipelago during the postglacial period. iii I dedicate this dissertation to my loving family. iv Acknowledgements I am grateful to all the Aleuts who participated in this study and provided the necessary DNA samples and family history information. I would also like to thank: Dr. Michael Crawford for his conceptualization of the Aleut Research Program at the University of Kansas and guidance provided for this dissertation project; Liza Mack for her boundless energy in promoting the project in the various Aleut communities; and Dr. Christine Hanson for welcoming the research team into her home. Without them this study would not have been possible. I would like to acknowledge my committee members for their valuable feedback on the research study: Dr. Michael Crawford, Dr. James Mielke, Dr. Alan Redd, Dr. Rolfe Mandel, and Dr. Steve Benedict. I would also like to thank my collaborators on this project: Dr. Rohina Rubicz, Dr. Mike Grose, and Dr. Katherine Reedy-Maschner; my fellow students: Phil Melton, Kristen Young, Orion Graf, Kristie Beaty, Geetha Chittoor, Anne Justice, Jennifer Rack, and Chris Phillips- Krawczak; the office staff: Judy Ross, Carol Archinal, and Kathleen Womack; and my family and friends for all their support. This research was funded by NSF grants #OPP-990690 and #OPP-0327676 awarded to Dr. Michael Crawford. v Table of Contents CHAPTER ONE: INTRODUCTION …………………………….…………………. 1 1 CHAPTER TWO: LITERATURE REVIEW …………………………………..…… 6 6 Anthropological Genetics Review …………………………………..………… 6 6 Early Research: From Classical to Molecular Markers ……................. 77 Mitochondrial DNA ……………..………………………...………….. 9 9 Y-Chromosome Markers ……………………………………………. 1818 Peopling of the Americas ……………………………….……………. 30 30 Population Background ………………………………………………………. 38 38 Archaeology and Prehistory …………………………………………. 40 Aleut Society at Russian Contact …………….……………………… 4747 Aleutian History ……………………………………………………… 50 50 Language …………………………………………………………….. 55 Morphology ………………………………………………………….. 5656 Genetics ……………………………………………………………… 5858 Summary …………………………………………………………………….. 63 CHAPTER THREE: MATERIALS AND METHODS …………………………… 6565 Sampling Methods …………………………………………………………… 6565 Laboratory Methods …………………………………………………………. 68 DNA Extraction ……………………………………………………… 6868 Mitochondrial DNA Analysis ………………….…………………….. 7070 Y-Chromosome Analysis ……………………….…………………… 78 Analytical Methods ………………………………………………………...... 82 Measures of Genetic Diversity ………………………………………. 8282 Neutrality Test Statistics ………………………….………………….. 83 83 Median-Joining Network Analysis …….…………………………….. 8686 Neighbor-Joining Trees …….…………………………….………….. 8989 Multidimensional Scaling ……………………………………………. 91 91 R-Matrix Analysis ……………………………...……………………. 9292 Heterozygosity versus rii …….……………………………………….. 94 94 Mismatch Distributions ……………………………………………… 9595 Estimates of Coalescence Time ……………………………………… 9797 Delaunay Triangulation ……………………………………………… 9999 Monmonier’s Maximum-Difference Algorithm …………..……....... 102 vi Genetic Landscape Interpolation ………………….….…………….. 103 Spatial Analysis of Molecular Variance ………….….….………….. 104 Mantel Test ………………………………………............................. 107107 Spatial Autocorrelation ………………….…….……………………. 108108 CHAPTER FOUR: RESULTS …………………………..……………………….. 110110 Mitochondrial DNA …………………………………..……………………. 110 HVS-I Sequencing and Haplogroup Frequencies ………..………… 110110 Spatial Autocorrelation and Mantel Testing ………………..………. 116116 Sequence Diversities and Neutrality Test Statistics ……….……...... 117 MtDNA Network Analysis …………………………………………. 120120 Neighbor-Joining Tree ………………………..……………………. 124124 R-Matrix Analysis …………………………………….……………. 126 Multidimensional Scaling and SAMOVA Analysis ………..………. 128128 Monmonier’s Maximum Difference Algorithm ……………………. 130 Genetic Surface Interpolation ………………………………………. 132 Diversity versus rii Plot ………………….…….……………………. 133133 Mismatch Distributions and Coalescent Time Estimations …...……. 135135 Y-Chromosome DNA …………………………….….…………………….. 138138 Y-Chromosome STR Haplotypes and Population Diversities ……… 138138 Y-Chromosome SNPs and Haplogroup Frequencies ………………. 141 Y-STR Network Analysis ………………………………………...... 144144 Neighbor-Joining Tree ……………………..………………………. 149149 Multidimensional Scaling …………………………………..………. 150150 R-Matrix Analysis ………………………………………….………. 151 Monmonier’s Maximum Difference Algorithm ……………………. 154 Genetic Surface Interpolation ………………………………………. 155 Diversity versus rii Plot ………………….….………………………. 157157 CHAPTER FIVE: DISCUSSION ……………………………..………………….. 159159 East-West Genetic Substructure ……………………….………………….... 160 Origins of the Aleut People ……………………………………………….... 166 CHAPTER SIX: CONCLUSION ……………………….….…………………...... 170170 LITERATURE CITED …………………………….………….………………….. 173173 APPENDIX A ……………………………………………….…………………… 208 APPENDIX B …………………………………………….….…………………… 209209 vii List of Figures Figure 1 Human Mitochondrial Genome ……………….………..………..……. 1010 Figure 2 Phylogeny of human mtDNA from five geographic regions …….……. 1515 Figure 3 Evolutionary migration patterns of human mtDNA haplogroups ….…. 17 Figure 4 Diagram of structural variation in the human Y-chromosome …….…. 1919 Figure 5 Pie charts of NRY haplogroup frequencies of global populations ……. 23 Figure 6 Differentiation of Y-chromosome macrohaplogroup F outside Africa ………………………………………………………………….. 25 Figure 7 Application of genetic markers in NRY and mtDNA phylogenetic reconstructions ……………………….………..………………………. 2828 Figure 8 Distribution of mtDNA haplogroup frequencies among Native
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