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Terminal Pleistocene Alaskan Genome Reveals First Founding Population of Native Americans J LETTER doi:10.1038/nature25173 Terminal Pleistocene Alaskan genome reveals first founding population of Native Americans J. Víctor Moreno-Mayar1*, Ben A. Potter2*, Lasse Vinner1*, Matthias Steinrücken3,4, Simon Rasmussen5, Jonathan Terhorst6,7, John A. Kamm6,8, Anders Albrechtsen9, Anna-Sapfo Malaspinas1,10,11, Martin Sikora1, Joshua D. Reuther2, Joel D. Irish12, Ripan S. Malhi13,14, Ludovic Orlando1, Yun S. Song6,15,16, Rasmus Nielsen1,6,17, David J. Meltzer1,18 & Eske Willerslev1,8,19 Despite broad agreement that the Americas were initially populated Native American ancestors were isolated from Asian groups in Beringia via Beringia, the land bridge that connected far northeast Asia before entering the Americas2,9,13; whether one or more early migra- with northwestern North America during the Pleistocene epoch, tions gave rise to the founding population of Native Americans1–4,7,14 when and how the peopling of the Americas occurred remains (it is commonly agreed that the Palaeo-Eskimos and Inuit populations unresolved1–5. Analyses of human remains from Late Pleistocene represent separate and later migrations1,15,16); and when and where Alaska are important to resolving the timing and dispersal of these the basal split between southern and northern Native American (SNA populations. The remains of two infants were recovered at Upward and NNA, respectively) branches occurred. It also remains unresolved Sun River (USR), and have been dated to around 11.5 thousand whether the genetic affinity between some SNA groups and indigenous years ago (ka)6. Here, by sequencing the USR1 genome to an average Australasians2,3 reflects migration by non-Native Americans3,4,14, early coverage of approximately 17 times, we show that USR1 is most population structure within the first Americans3 or later gene flow2. To closely related to Native Americans, but falls basal to all previously resolve these uncertainties, a better understanding of the population sequenced contemporary and ancient Native Americans1,7,8. As history of Beringia, the entryway for the Pleistocene peopling of the such, USR1 represents a distinct Ancient Beringian population. Americas, is needed. Using demographic modelling, we infer that the Ancient Beringian Genomic insight into that population history has now become population and ancestors of other Native Americans descended available with the recently recovered infant remains (USR1 and USR2) from a single founding population that initially split from East from the Upward Sun River site, Alaska (eastern Beringia), which have Asians around 36 ± 1.5 ka, with gene flow persisting until around been dated to approximately 11.5 ka6,17. Mitochondrial DNA sequences 25 ± 1.1 ka. Gene flow from ancient north Eurasians into all Native (haplogroups C1 and B2, respectively) were previously acquired from Americans took place 25–20 ka, with Ancient Beringians branching these individuals6,17 (Supplementary Information sections 1, 4.5). We off around 22–18.1 ka. Our findings support a long-term genetic have since obtained whole-genome sequence data, which provide a structure in ancestral Native Americans, consistent with the broader opportunity to investigate the number, source(s) and structure Beringian ‘standstill model’9. We show that the basal northern of the initial founding population(s) and the timing and location of and southern Native American branches, to which all other Native their subsequent divergence. We sequenced the genome of USR1 to an Americans belong, diverged around 17.5–14.6 ka, and that this average depth of approximately 17× , on the basis of eight sequencing probably occurred south of the North American ice sheets. We libraries from uracil-specific excision reagent-treated extracts that also show that after 11.5 ka, some of the northern Native American had previously been confirmed to contain DNA fragments with char- populations received gene flow from a Siberian population most acteristic ancient DNA misincorporation patterns (Supplementary closely related to Koryaks, but not Palaeo-Eskimos1, Inuits or Information sections 2–4). We estimated modern human contami- Kets10, and that Native American gene flow into Inuits was through nation to be around 0.14% based on the nuclear genome and about northern and not southern Native American groups1. Our findings 0.15% based on mitochondrial DNA (Supplementary Information further suggest that the far-northern North American presence of section 4). As expected, the error rate in the uracil-specific excision northern Native Americans is from a back migration that replaced reagent-treated sequencing data was low (0.09% errors per base), and or absorbed the initial founding population of Ancient Beringians. comparable to other high-coverage contemporary genomes, based on The details of the peopling of the Americas, and particularly the called genotypes (Supplementary Information section 4). Although population history of Beringia, remain unresolved2,3. Humans were USR26 did not have sufficient endogenous DNA for high-coverage present in the Americas south of the continental ice sheets by around genome sequencing, we found that both individuals were close relatives 14.6 ka11, indicating that they traversed Beringia earlier. During the (Supplementary Information section 5), equally related to worldwide Last Glacial Maximum (LGM), this region was marked by harsh cli- present-day populations (Supplementary Fig. 4g). mates and glacial barriers5, which may have led to the isolation of We assessed the genetic relationship between USR1, a set of ancient populations for extended periods, and at times complicated dispersal genomes2,7,8,14,16 and a panel of 167 worldwide populations genotyped across the region12. It remains unknown whether and for how long for 199,285 single-nucleotide polymorphisms1,2,18 (Supplementary 1Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 Copenhagen, Denmark. 2Department of Anthropology, University of Alaska, Fairbanks, Alaska 99775, USA. 3Department of Biostatistics and Epidemiology, University of Massachusetts, Amherst, Massachusetts 01003, USA. 4Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA. 5Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Kongens Lyngby, Denmark. 6Department of Statistics, University of California, Berkeley, California 94720, USA. 7Department of Statistics, University of Michigan, Ann Arbor, Michigan 48109, USA. 8Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK. 9The Bioinformatics Centre, Department of Biology, University of Copenhagen, 2200 Copenhagen, Denmark. 10Department of Computational Biology, University of Lausanne, Lausanne, Switzerland. 11Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland. 12Research Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores University, Liverpool L3 3AF, UK. 13Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA. 14Carle R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA. 15Computer Science Division, University of California, Berkeley, California 94720, USA. 16Chan Zuckerberg Biohub, San Francisco, California 94158, USA. 17Department of Integrative Biology, University of California, Berkeley, California 94720, USA. 18Department of Anthropology, Southern Methodist University, Dallas, Texas 75275, USA. 19Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. *These authors contributed equally to this work. 11 JANUARY 2018 | VOL 553 | NATURE | 203 © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. RESEARCH LETTER D < 0 D = 0 D > 0 a b USR1 USR1 USR1 USR1 Yoruba Yoruba Yoruba Aymara Aymara Aymara Nat.Am. Nat.Am. Nat.Am. Karitiana Guahibo Surui Parakana Chane Equatorial Palikur Guarani Tucanoan Ticuna Jamamadi Piapoco Wayuu Yaghan 3 Chilote 0.25 0.28 0. 0.33 0.36 0.38 Inga Quechua Andean f3(San; X, USR1) Chono Huilliche Diaguita Guaymi Z score for Waunana c Teribe D(Aymara, Nat. Am.; Han, YRI) Cabecar –2.5 0 2.5 5.0 Kogi Chibchan Maleku Embera Paezan Bribri Purepecha Equatorial Chibchan Andean Arhuaco Tucanoan Paezan Huetar Arara Wichi Ge−Pano 10 Toba Caribbean 5 Kaingang USAmerindian_2 0 USAmerindian_3 Mixtec –5 Huichol Central Yaqui –10 Zapotec2 Amerind Zapotec1 –15 Tepehuano Pima Ge−Pano Central Northern USAmerindian_1 Caribbean Amerind Amerind Maya Mixe Cucupa 10 USAmerindian_4 Kaqchikel 5 Algonquin scores for 0 Kumlai Z Maya1 Northern –5 Maya2 Cree Amerind –10 Coastal_Tsimshian Cochimi –15 Stswecemc Ojibwa* Observed Eskimo Nisgaa NaDene H0 Splatsin Aleut CanAmerindian_*1 (Nat. Am., USR1; Sib. 1, 2) InteriorTsimshian D 10 Northern_Athabascans_4 Southern_Athabascans_1 5 Haida 1 2 Chipewyan 0 Northern_Athabascans_2* NaDene Tlingit Sib. Sib. –5 USR1 Northern_Athabascans_1* Northern_Athabascans_3 –10 Nat. Am. Aleutians –15 West_Greenlanders* Eskimo –4 –2 0 24–4 –2 0 24–4 –2 0 24 East_Greenlanders* Alaskan_Inuit* Aleut Expected Z scores for * –0.050 –0.025 0 0.025 0.050 D(Nat. Am., USR1; Sib. 1, Sib. 2) d D(Nat. Am., Aymara; USR1, Yoruba) r a i t h d n 9 Ke vk in 93 Altaic Ni bean Malta Afric Europe ib ndean newick USR1 Oceania NaDene A Saqqaqn Anzick1 Near East Caucasus East Asia South Asia lic−Yukagh Ke a Eskimo Aleut ial Tucanoan Southeast Asia Ur Central Amer Northern Amerind Chibchan−Paeza EquatorGe−Pano Car
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