Publications by authors named "Nicole Adamski"

14 Publications

  • Page 1 of 1

Genomic insights into the formation of human populations in East Asia.

Nature 2021 Mar 22;591(7850):413-419. Epub 2021 Feb 22.

Department of Genetics, Harvard Medical School, Boston, MA, USA.

The deep population history of East Asia remains poorly understood owing to a lack of ancient DNA data and sparse sampling of present-day people. Here we report genome-wide data from 166 East Asian individuals dating to between 6000 BC and AD 1000 and 46 present-day groups. Hunter-gatherers from Japan, the Amur River Basin, and people of Neolithic and Iron Age Taiwan and the Tibetan Plateau are linked by a deeply splitting lineage that probably reflects a coastal migration during the Late Pleistocene epoch. We also follow expansions during the subsequent Holocene epoch from four regions. First, hunter-gatherers from Mongolia and the Amur River Basin have ancestry shared by individuals who speak Mongolic and Tungusic languages, but do not carry ancestry characteristic of farmers from the West Liao River region (around 3000 BC), which contradicts theories that the expansion of these farmers spread the Mongolic and Tungusic proto-languages. Second, farmers from the Yellow River Basin (around 3000 BC) probably spread Sino-Tibetan languages, as their ancestry dispersed both to Tibet-where it forms approximately 84% of the gene pool in some groups-and to the Central Plain, where it has contributed around 59-84% to modern Han Chinese groups. Third, people from Taiwan from around 1300 BC to AD 800 derived approximately 75% of their ancestry from a lineage that is widespread in modern individuals who speak Austronesian, Tai-Kadai and Austroasiatic languages, and that we hypothesize derives from farmers of the Yangtze River Valley. Ancient people from Taiwan also derived about 25% of their ancestry from a northern lineage that is related to, but different from, farmers of the Yellow River Basin, which suggests an additional north-to-south expansion. Fourth, ancestry from Yamnaya Steppe pastoralists arrived in western Mongolia after around 3000 BC but was displaced by previously established lineages even while it persisted in western China, as would be expected if this ancestry was associated with the spread of proto-Tocharian Indo-European languages. Two later gene flows affected western Mongolia: migrants after around 2000 BC with Yamnaya and European farmer ancestry, and episodic influences of later groups with ancestry from Turan.
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http://dx.doi.org/10.1038/s41586-021-03336-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7993749PMC
March 2021

A minimally destructive protocol for DNA extraction from ancient teeth.

Genome Res 2021 Mar 12;31(3):472-483. Epub 2021 Feb 12.

Department of Evolutionary Anthropology, University of Vienna, Vienna 1090, Austria.

Ancient DNA sampling methods-although optimized for efficient DNA extraction-are destructive, relying on drilling or cutting and powdering (parts of) bones and teeth. As the field of ancient DNA has grown, so have concerns about the impact of destructive sampling of the skeletal remains from which ancient DNA is obtained. Due to a particularly high concentration of endogenous DNA, the cementum of tooth roots is often targeted for ancient DNA sampling, but destructive sampling methods of the cementum often result in the loss of at least one entire root. Here, we present a minimally destructive method for extracting ancient DNA from dental cementum present on the surface of tooth roots. This method does not require destructive drilling or grinding, and, following extraction, the tooth remains safe to handle and suitable for most morphological studies, as well as other biochemical studies, such as radiocarbon dating. We extracted and sequenced ancient DNA from 30 teeth (and nine corresponding petrous bones) using this minimally destructive extraction method in addition to a typical tooth sampling method. We find that the minimally destructive method can provide ancient DNA that is of comparable quality to extracts produced from teeth that have undergone destructive sampling processes. Further, we find that a rigorous cleaning of the tooth surface combining diluted bleach and UV light irradiation seems sufficient to minimize external contaminants usually removed through the physical removal of a superficial layer when sampling through regular powdering methods.
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http://dx.doi.org/10.1101/gr.267534.120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7919446PMC
March 2021

A genetic history of the pre-contact Caribbean.

Nature 2021 02 23;590(7844):103-110. Epub 2020 Dec 23.

Department of Genetics, Harvard Medical School, Boston, MA, USA.

Humans settled the Caribbean about 6,000 years ago, and ceramic use and intensified agriculture mark a shift from the Archaic to the Ceramic Age at around 2,500 years ago. Here we report genome-wide data from 174 ancient individuals from The Bahamas, Haiti and the Dominican Republic (collectively, Hispaniola), Puerto Rico, Curaçao and Venezuela, which we co-analysed with 89 previously published ancient individuals. Stone-tool-using Caribbean people, who first entered the Caribbean during the Archaic Age, derive from a deeply divergent population that is closest to Central and northern South American individuals; contrary to previous work, we find no support for ancestry contributed by a population related to North American individuals. Archaic-related lineages were >98% replaced by a genetically homogeneous ceramic-using population related to speakers of languages in the Arawak family from northeast South America; these people moved through the Lesser Antilles and into the Greater Antilles at least 1,700 years ago, introducing ancestry that is still present. Ancient Caribbean people avoided close kin unions despite limited mate pools that reflect small effective population sizes, which we estimate to be a minimum of 500-1,500 and a maximum of 1,530-8,150 individuals on the combined islands of Puerto Rico and Hispaniola in the dozens of generations before the individuals who we analysed lived. Census sizes are unlikely to be more than tenfold larger than effective population sizes, so previous pan-Caribbean estimates of hundreds of thousands of people are too large. Confirming a small and interconnected Ceramic Age population, we detect 19 pairs of cross-island cousins, close relatives buried around 75 km apart in Hispaniola and low genetic differentiation across islands. Genetic continuity across transitions in pottery styles reveals that cultural changes during the Ceramic Age were not driven by migration of genetically differentiated groups from the mainland, but instead reflected interactions within an interconnected Caribbean world.
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http://dx.doi.org/10.1038/s41586-020-03053-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7864882PMC
February 2021

Ancient genomes in South Patagonia reveal population movements associated with technological shifts and geography.

Nat Commun 2020 08 3;11(1):3868. Epub 2020 Aug 3.

Department of Genetics, Harvard Medical School, Boston, MA, 02115, USA.

Archaeological research documents major technological shifts among people who have lived in the southern tip of South America (South Patagonia) during the last thirteen millennia, including the development of marine-based economies and changes in tools and raw materials. It has been proposed that movements of people spreading culture and technology propelled some of these shifts, but these hypotheses have not been tested with ancient DNA. Here we report genome-wide data from 20 ancient individuals, and co-analyze it with previously reported data. We reveal that immigration does not explain the appearance of marine adaptations in South Patagonia. We describe partial genetic continuity since ~6600 BP and two later gene flows correlated with technological changes: one between 4700-2000 BP that affected primarily marine-based groups, and a later one impacting all <2000 BP groups. From ~2200-1200 BP, mixture among neighbors resulted in a cline correlated to geographic ordering along the coast.
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http://dx.doi.org/10.1038/s41467-020-17656-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7400565PMC
August 2020

The Genomic History of the Bronze Age Southern Levant.

Cell 2020 05;181(5):1146-1157.e11

Department of Genetics, Harvard Medical School, Boston, MA 02115, USA; Broad Institute, Cambridge, MA 02138, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA; Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address:

We report genome-wide DNA data for 73 individuals from five archaeological sites across the Bronze and Iron Ages Southern Levant. These individuals, who share the "Canaanite" material culture, can be modeled as descending from two sources: (1) earlier local Neolithic populations and (2) populations related to the Chalcolithic Zagros or the Bronze Age Caucasus. The non-local contribution increased over time, as evinced by three outliers who can be modeled as descendants of recent migrants. We show evidence that different "Canaanite" groups genetically resemble each other more than other populations. We find that Levant-related modern populations typically have substantial ancestry coming from populations related to the Chalcolithic Zagros and the Bronze Age Southern Levant. These groups also harbor ancestry from sources we cannot fully model with the available data, highlighting the critical role of post-Bronze-Age migrations into the region over the past 3,000 years.
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http://dx.doi.org/10.1016/j.cell.2020.04.024DOI Listing
May 2020

Human auditory ossicles as an alternative optimal source of ancient DNA.

Genome Res 2020 03 25;30(3):427-436. Epub 2020 Feb 25.

Department of Evolutionary Anthropology, University of Vienna, Vienna, 1090, Austria.

DNA recovery from ancient human remains has revolutionized our ability to reconstruct the genetic landscape of the past. Ancient DNA research has benefited from the identification of skeletal elements, such as the cochlear part of the osseous inner ear, that provides optimal contexts for DNA preservation; however, the rich genetic information obtained from the cochlea must be counterbalanced against the loss of morphological information caused by its sampling. Motivated by similarities in developmental processes and histological properties between the cochlea and auditory ossicles, we evaluate the ossicles as an alternative source of ancient DNA. We show that ossicles perform comparably to the cochlea in terms of DNA recovery, finding no substantial reduction in data quantity and minimal differences in data quality across preservation conditions. Ossicles can be sampled from intact skulls or disarticulated petrous bones without damage to surrounding bone, and we argue that they should be used when available to reduce damage to human remains. Our results identify another optimal skeletal element for ancient DNA analysis and add to a growing toolkit of sampling methods that help to better preserve skeletal remains for future research while maximizing the likelihood that ancient DNA analysis will produce useable results.
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http://dx.doi.org/10.1101/gr.260141.119DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7111520PMC
March 2020

Ancient West African foragers in the context of African population history.

Nature 2020 01 22;577(7792):665-670. Epub 2020 Jan 22.

Department of Genetics, Harvard Medical School, Boston, MA, USA.

Our knowledge of ancient human population structure in sub-Saharan Africa, particularly prior to the advent of food production, remains limited. Here we report genome-wide DNA data from four children-two of whom were buried approximately 8,000 years ago and two 3,000 years ago-from Shum Laka (Cameroon), one of the earliest known archaeological sites within the probable homeland of the Bantu language group. One individual carried the deeply divergent Y chromosome haplogroup A00, which today is found almost exclusively in the same region. However, the genome-wide ancestry profiles of all four individuals are most similar to those of present-day hunter-gatherers from western Central Africa, which implies that populations in western Cameroon today-as well as speakers of Bantu languages from across the continent-are not descended substantially from the population represented by these four people. We infer an Africa-wide phylogeny that features widespread admixture and three prominent radiations, including one that gave rise to at least four major lineages deep in the history of modern humans.
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http://dx.doi.org/10.1038/s41586-020-1929-1DOI Listing
January 2020

An Ancient Harappan Genome Lacks Ancestry from Steppe Pastoralists or Iranian Farmers.

Cell 2019 10 5;179(3):729-735.e10. Epub 2019 Sep 5.

Department of Genetics, Harvard Medical School, Boston, MA 02115, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA. Electronic address:

We report an ancient genome from the Indus Valley Civilization (IVC). The individual we sequenced fits as a mixture of people related to ancient Iranians (the largest component) and Southeast Asian hunter-gatherers, a unique profile that matches ancient DNA from 11 genetic outliers from sites in Iran and Turkmenistan in cultural communication with the IVC. These individuals had little if any Steppe pastoralist-derived ancestry, showing that it was not ubiquitous in northwest South Asia during the IVC as it is today. The Iranian-related ancestry in the IVC derives from a lineage leading to early Iranian farmers, herders, and hunter-gatherers before their ancestors separated, contradicting the hypothesis that the shared ancestry between early Iranians and South Asians reflects a large-scale spread of western Iranian farmers east. Instead, sampled ancient genomes from the Iranian plateau and IVC descend from different groups of hunter-gatherers who began farming without being connected by substantial movement of people.
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http://dx.doi.org/10.1016/j.cell.2019.08.048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6800651PMC
October 2019

The formation of human populations in South and Central Asia.

Authors:
Vagheesh M Narasimhan Nick Patterson Priya Moorjani Nadin Rohland Rebecca Bernardos Swapan Mallick Iosif Lazaridis Nathan Nakatsuka Iñigo Olalde Mark Lipson Alexander M Kim Luca M Olivieri Alfredo Coppa Massimo Vidale James Mallory Vyacheslav Moiseyev Egor Kitov Janet Monge Nicole Adamski Neel Alex Nasreen Broomandkhoshbacht Francesca Candilio Kimberly Callan Olivia Cheronet Brendan J Culleton Matthew Ferry Daniel Fernandes Suzanne Freilich Beatriz Gamarra Daniel Gaudio Mateja Hajdinjak Éadaoin Harney Thomas K Harper Denise Keating Ann Marie Lawson Matthew Mah Kirsten Mandl Megan Michel Mario Novak Jonas Oppenheimer Niraj Rai Kendra Sirak Viviane Slon Kristin Stewardson Fatma Zalzala Zhao Zhang Gaziz Akhatov Anatoly N Bagashev Alessandra Bagnera Bauryzhan Baitanayev Julio Bendezu-Sarmiento Arman A Bissembaev Gian Luca Bonora Temirlan T Chargynov Tatiana Chikisheva Petr K Dashkovskiy Anatoly Derevianko Miroslav Dobeš Katerina Douka Nadezhda Dubova Meiram N Duisengali Dmitry Enshin Andrey Epimakhov Alexey V Fribus Dorian Fuller Alexander Goryachev Andrey Gromov Sergey P Grushin Bryan Hanks Margaret Judd Erlan Kazizov Aleksander Khokhlov Aleksander P Krygin Elena Kupriyanova Pavel Kuznetsov Donata Luiselli Farhod Maksudov Aslan M Mamedov Talgat B Mamirov Christopher Meiklejohn Deborah C Merrett Roberto Micheli Oleg Mochalov Samariddin Mustafokulov Ayushi Nayak Davide Pettener Richard Potts Dmitry Razhev Marina Rykun Stefania Sarno Tatyana M Savenkova Kulyan Sikhymbaeva Sergey M Slepchenko Oroz A Soltobaev Nadezhda Stepanova Svetlana Svyatko Kubatbek Tabaldiev Maria Teschler-Nicola Alexey A Tishkin Vitaly V Tkachev Sergey Vasilyev Petr Velemínský Dmitriy Voyakin Antonina Yermolayeva Muhammad Zahir Valery S Zubkov Alisa Zubova Vasant S Shinde Carles Lalueza-Fox Matthias Meyer David Anthony Nicole Boivin Kumarasamy Thangaraj Douglas J Kennett Michael Frachetti Ron Pinhasi David Reich

Science 2019 09;365(6457)

Department of Genetics, Harvard Medical School, Boston, MA 02115, USA.

By sequencing 523 ancient humans, we show that the primary source of ancestry in modern South Asians is a prehistoric genetic gradient between people related to early hunter-gatherers of Iran and Southeast Asia. After the Indus Valley Civilization's decline, its people mixed with individuals in the southeast to form one of the two main ancestral populations of South Asia, whose direct descendants live in southern India. Simultaneously, they mixed with descendants of Steppe pastoralists who, starting around 4000 years ago, spread via Central Asia to form the other main ancestral population. The Steppe ancestry in South Asia has the same profile as that in Bronze Age Eastern Europe, tracking a movement of people that affected both regions and that likely spread the distinctive features shared between Indo-Iranian and Balto-Slavic languages.
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http://dx.doi.org/10.1126/science.aat7487DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6822619PMC
September 2019

Ancient DNA from the skeletons of Roopkund Lake reveals Mediterranean migrants in India.

Nat Commun 2019 08 20;10(1):3670. Epub 2019 Aug 20.

CSIR Centre for Cellular and Molecular Biology, Hyderabad, Telangana, 500007, India.

Situated at over 5,000 meters above sea level in the Himalayan Mountains, Roopkund Lake is home to the scattered skeletal remains of several hundred individuals of unknown origin. We report genome-wide ancient DNA for 38 skeletons from Roopkund Lake, and find that they cluster into three distinct groups. A group of 23 individuals have ancestry that falls within the range of variation of present-day South Asians. A further 14 have ancestry typical of the eastern Mediterranean. We also identify one individual with Southeast Asian-related ancestry. Radiocarbon dating indicates that these remains were not deposited simultaneously. Instead, all of the individuals with South Asian-related ancestry date to ~800 CE (but with evidence of being deposited in more than one event), while all other individuals date to ~1800 CE. These differences are also reflected in stable isotope measurements, which reveal a distinct dietary profile for the two main groups.
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http://dx.doi.org/10.1038/s41467-019-11357-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6702210PMC
August 2019

Palaeo-Eskimo genetic ancestry and the peopling of Chukotka and North America.

Nature 2019 06 5;570(7760):236-240. Epub 2019 Jun 5.

Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, Germany.

Much of the American Arctic was first settled 5,000 years ago, by groups of people known as Palaeo-Eskimos. They were subsequently joined and largely displaced around 1,000 years ago by ancestors of the present-day Inuit and Yup'ik. The genetic relationship between Palaeo-Eskimos and Native American, Inuit, Yup'ik and Aleut populations remains uncertain. Here we present genomic data for 48 ancient individuals from Chukotka, East Siberia, the Aleutian Islands, Alaska, and the Canadian Arctic. We co-analyse these data with data from present-day Alaskan Iñupiat and West Siberian populations and published genomes. Using methods based on rare-allele and haplotype sharing, as well as established techniques, we show that Palaeo-Eskimo-related ancestry is ubiquitous among people who speak Na-Dene and Eskimo-Aleut languages. We develop a comprehensive model for the Holocene peopling events of Chukotka and North America, and show that Na-Dene-speaking peoples, people of the Aleutian Islands, and Yup'ik and Inuit across the Arctic region all share ancestry from a single Palaeo-Eskimo-related Siberian source.
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http://dx.doi.org/10.1038/s41586-019-1251-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6942545PMC
June 2019

Ancient DNA reveals a multistep spread of the first herders into sub-Saharan Africa.

Science 2019 07 30;365(6448). Epub 2019 May 30.

Department of Genetics, Harvard Medical School, Boston, MA 02115, USA.

How food production first entered eastern Africa ~5000 years ago and the extent to which people moved with livestock is unclear. We present genome-wide data from 41 individuals associated with Later Stone Age, Pastoral Neolithic (PN), and Iron Age contexts in what are now Kenya and Tanzania to examine the genetic impacts of the spreads of herding and farming. Our results support a multiphase model in which admixture between northeastern African-related peoples and eastern African foragers formed multiple pastoralist groups, including a genetically homogeneous PN cluster. Additional admixture with northeastern and western African-related groups occurred by the Iron Age. These findings support several movements of food producers while rejecting models of minimal admixture with foragers and of genetic differentiation between makers of distinct PN artifacts.
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http://dx.doi.org/10.1126/science.aaw6275DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6827346PMC
July 2019

The genomic history of the Iberian Peninsula over the past 8000 years.

Authors:
Iñigo Olalde Swapan Mallick Nick Patterson Nadin Rohland Vanessa Villalba-Mouco Marina Silva Katharina Dulias Ceiridwen J Edwards Francesca Gandini Maria Pala Pedro Soares Manuel Ferrando-Bernal Nicole Adamski Nasreen Broomandkhoshbacht Olivia Cheronet Brendan J Culleton Daniel Fernandes Ann Marie Lawson Matthew Mah Jonas Oppenheimer Kristin Stewardson Zhao Zhang Juan Manuel Jiménez Arenas Isidro Jorge Toro Moyano Domingo C Salazar-García Pere Castanyer Marta Santos Joaquim Tremoleda Marina Lozano Pablo García Borja Javier Fernández-Eraso José Antonio Mujika-Alustiza Cecilio Barroso Francisco J Bermúdez Enrique Viguera Mínguez Josep Burch Neus Coromina David Vivó Artur Cebrià Josep Maria Fullola Oreto García-Puchol Juan Ignacio Morales F Xavier Oms Tona Majó Josep Maria Vergès Antònia Díaz-Carvajal Imma Ollich-Castanyer F Javier López-Cachero Ana Maria Silva Carmen Alonso-Fernández Germán Delibes de Castro Javier Jiménez Echevarría Adolfo Moreno-Márquez Guillermo Pascual Berlanga Pablo Ramos-García José Ramos-Muñoz Eduardo Vijande Vila Gustau Aguilella Arzo Ángel Esparza Arroyo Katina T Lillios Jennifer Mack Javier Velasco-Vázquez Anna Waterman Luis Benítez de Lugo Enrich María Benito Sánchez Bibiana Agustí Ferran Codina Gabriel de Prado Almudena Estalrrich Álvaro Fernández Flores Clive Finlayson Geraldine Finlayson Stewart Finlayson Francisco Giles-Guzmán Antonio Rosas Virginia Barciela González Gabriel García Atiénzar Mauro S Hernández Pérez Armando Llanos Yolanda Carrión Marco Isabel Collado Beneyto David López-Serrano Mario Sanz Tormo António C Valera Concepción Blasco Corina Liesau Patricia Ríos Joan Daura María Jesús de Pedro Michó Agustín A Diez-Castillo Raúl Flores Fernández Joan Francès Farré Rafael Garrido-Pena Victor S Gonçalves Elisa Guerra-Doce Ana Mercedes Herrero-Corral Joaquim Juan-Cabanilles Daniel López-Reyes Sarah B McClure Marta Merino Pérez Arturo Oliver Foix Montserrat Sanz Borràs Ana Catarina Sousa Julio Manuel Vidal Encinas Douglas J Kennett Martin B Richards Kurt Werner Alt Wolfgang Haak Ron Pinhasi Carles Lalueza-Fox David Reich

Science 2019 03;363(6432):1230-1234

Department of Genetics, Harvard Medical School, Boston, MA, USA.

We assembled genome-wide data from 271 ancient Iberians, of whom 176 are from the largely unsampled period after 2000 BCE, thereby providing a high-resolution time transect of the Iberian Peninsula. We document high genetic substructure between northwestern and southeastern hunter-gatherers before the spread of farming. We reveal sporadic contacts between Iberia and North Africa by ~2500 BCE and, by ~2000 BCE, the replacement of 40% of Iberia's ancestry and nearly 100% of its Y-chromosomes by people with Steppe ancestry. We show that, in the Iron Age, Steppe ancestry had spread not only into Indo-European-speaking regions but also into non-Indo-European-speaking ones, and we reveal that present-day Basques are best described as a typical Iron Age population without the admixture events that later affected the rest of Iberia. Additionally, we document how, beginning at least in the Roman period, the ancestry of the peninsula was transformed by gene flow from North Africa and the eastern Mediterranean.
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http://dx.doi.org/10.1126/science.aav4040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436108PMC
March 2019

Reconstructing the Deep Population History of Central and South America.

Cell 2018 11 8;175(5):1185-1197.e22. Epub 2018 Nov 8.

Department of Genetics, Harvard Medical School, Boston, MA 02115, USA; Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA; Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA. Electronic address:

We report genome-wide ancient DNA from 49 individuals forming four parallel time transects in Belize, Brazil, the Central Andes, and the Southern Cone, each dating to at least ∼9,000 years ago. The common ancestral population radiated rapidly from just one of the two early branches that contributed to Native Americans today. We document two previously unappreciated streams of gene flow between North and South America. One affected the Central Andes by ∼4,200 years ago, while the other explains an affinity between the oldest North American genome associated with the Clovis culture and the oldest Central and South Americans from Chile, Brazil, and Belize. However, this was not the primary source for later South Americans, as the other ancient individuals derive from lineages without specific affinity to the Clovis-associated genome, suggesting a population replacement that began at least 9,000 years ago and was followed by substantial population continuity in multiple regions.
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http://dx.doi.org/10.1016/j.cell.2018.10.027DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6327247PMC
November 2018