The Genomic Impact of European Colonization of the Americas

doi:10.1016/j.cub.2019.09.076

. 2019 Dec 2;29(23):3974-3986.e4.

doi: 10.1016/j.cub.2019.09.076. Epub 2019 Nov 14.

The Genomic Impact of European Colonization of the Americas

Linda Ongaro¹, Marilia O Scliar², Rodrigo Flores³, Alessandro Raveane⁴, Davide Marnetto³, Stefania Sarno⁵, Guido A Gnecchi-Ruscone⁶, Marta E Alarcón-Riquelme⁷, Etienne Patin⁸, Pongsakorn Wangkumhang⁹, Garrett Hellenthal⁹, Miguel Gonzalez-Santos¹⁰, Roy J King¹¹, Anastasia Kouvatsi¹², Oleg Balanovsky¹³, Elena Balanovska¹³, Lubov Atramentova¹⁴, Shahlo Turdikulova¹⁵, Sarabjit Mastana¹⁶, Damir Marjanovic¹⁷, Lejla Mulahasanovic¹⁸, Andreja Leskovac¹⁹, Maria F Lima-Costa²⁰, Alexandre C Pereira²¹, Mauricio L Barreto²², Bernardo L Horta²³, Nédio Mabunda²⁴, Celia A May²⁵, Andrés Moreno-Estrada²⁶, Alessandro Achilli⁴, Anna Olivieri⁴, Ornella Semino⁴, Kristiina Tambets³, Toomas Kivisild²⁷, Donata Luiselli²⁸, Antonio Torroni⁴, Cristian Capelli¹⁰, Eduardo Tarazona-Santos²⁹, Mait Metspalu³, Luca Pagani³⁰, Francesco Montinaro³¹

Affiliations

¹ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Evolutionary Biology, Institute of Molecular and Cell Biology, Riia 23, Tartu 51010, Estonia. Electronic address: linda.ongaro@ut.ee.
² Human Genome and Stem Cell Research Center, Biosciences Institute, University of São Paulo, São Paulo, SP 05508-090, Brazil; Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
³ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia.
⁴ Department of Biology and Biotechnology "L. Spallanzani", University of Pavia, Pavia 27100, Italy.
⁵ Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna 40100, Italy.
⁶ Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna 40100, Italy; Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena 07745, Germany.
⁷ GENYO, Centre for Genomics and Oncological Research, Pfizer/University of Granada/Andalusian Regional Government, Granada 18016, Spain.
⁸ Human Evolutionary Genetics Unit, Pasteur Institute, UMR2000, CNRS, Paris 75015, France.
⁹ Department of Genetics, Evolution and Environment and UCL Genetics Institute, University College London, London WC1E 6BT, UK.
¹⁰ Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK.
¹¹ Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA 94305-5101, USA.
¹² Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece.
¹³ Vavilov Institute of General Genetics, Ulitsa Gubkina, 3, Moscow 117971, Russia; Research Centre for Medical Genetics, Moskvorech'ye Ulitsa, 1, Moscow 115478, Russia; Biobank of North Eurasia, Kotlyakovskaya Ulitsa, 3 строение 12, Moscow 115201, Russia.
¹⁴ Department of Genetics and Cytology, V.N. Karazin Kharkiv National University, Kharkiv 61022, Ukraine.
¹⁵ Laboratory of Genomics, Institute of Bioorganic Chemistry, Academy of Sciences Republic of Uzbekistan, Tashkent 100047, Uzbekistan.
¹⁶ School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough LE11 3TU, UK.
¹⁷ Department of Genetics and Bioengineering, Faculty of Engineering and Information Technologies, International Burch University, Sarajevo 71000, Bosnia and Herzegovina; Institute for Anthropological Researches, Zagreb, Croatia.
¹⁸ CeGaT GmbH, Tübingen, Praxis für Humangenetik, Tübingen 72076, Germany.
¹⁹ Vinca Institute of Nuclear Sciences, University of Belgrade, M. Petrovica Alasa 12-14, Belgrade 11001, Serbia.
²⁰ Instituto de Pesquisa Rene Rachou, Fundação Oswaldo Cruz, Belo Horizonte, MG 30190-002, Brazil.
²¹ Instituto do Coração, Universidade de São Paulo, São Paulo, SP 05403-900, Brazil.
²² Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, BA 0110-040, Brazil; Center of Data and Knowledge Integration for Health (CIDACS), Fundação Oswaldo Cruz (FIOCRUZ), Salvador, BA 41745-715, Brazil.
²³ Programa de Pós-Graduação em Epidemiologia, Universidade Federal de Pelotas, 464, Pelotas, RS 96001-970, Brazil.
²⁴ Instituto Nacional de Saúde, Distrito de Marracuene, Estrada Nacional N 1, Província de Maputo, Maputo 1120, Mozambique.
²⁵ Department of Genetics & Genome Biology, University of Leicester, Leicester LE1 7RH, UK.
²⁶ National Laboratory of Genomics for Biodiversity (LANGEBIO), CINVESTAV, Irapuato, Guanajuato 36821, Mexico.
²⁷ Department of Human Genetics, KU Leuven, Herestraat 49 - box 602, Leuven 3000, Belgium.
²⁸ Department of Cultural Heritage, University of Bologna, Ravenna Campus, Ravenna 48100, Italy.
²⁹ Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
³⁰ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Biology, University of Padua, Via Ugo Bassi 58B, Padua 35100, Italy.
³¹ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK. Electronic address: francesco.montinaro@gmail.com.

PMID: 31735679
DOI: 10.1016/j.cub.2019.09.076

Free article

The Genomic Impact of European Colonization of the Americas

Linda Ongaro et al. Curr Biol. 2019.

Free article

. 2019 Dec 2;29(23):3974-3986.e4.

doi: 10.1016/j.cub.2019.09.076. Epub 2019 Nov 14.

Authors

Affiliations

¹ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Evolutionary Biology, Institute of Molecular and Cell Biology, Riia 23, Tartu 51010, Estonia. Electronic address: linda.ongaro@ut.ee.
² Human Genome and Stem Cell Research Center, Biosciences Institute, University of São Paulo, São Paulo, SP 05508-090, Brazil; Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
³ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia.
⁴ Department of Biology and Biotechnology "L. Spallanzani", University of Pavia, Pavia 27100, Italy.
⁵ Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna 40100, Italy.
⁶ Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna 40100, Italy; Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena 07745, Germany.
⁷ GENYO, Centre for Genomics and Oncological Research, Pfizer/University of Granada/Andalusian Regional Government, Granada 18016, Spain.
⁸ Human Evolutionary Genetics Unit, Pasteur Institute, UMR2000, CNRS, Paris 75015, France.
⁹ Department of Genetics, Evolution and Environment and UCL Genetics Institute, University College London, London WC1E 6BT, UK.
¹⁰ Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK.
¹¹ Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA 94305-5101, USA.
¹² Department of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece.
¹³ Vavilov Institute of General Genetics, Ulitsa Gubkina, 3, Moscow 117971, Russia; Research Centre for Medical Genetics, Moskvorech'ye Ulitsa, 1, Moscow 115478, Russia; Biobank of North Eurasia, Kotlyakovskaya Ulitsa, 3 строение 12, Moscow 115201, Russia.
¹⁴ Department of Genetics and Cytology, V.N. Karazin Kharkiv National University, Kharkiv 61022, Ukraine.
¹⁵ Laboratory of Genomics, Institute of Bioorganic Chemistry, Academy of Sciences Republic of Uzbekistan, Tashkent 100047, Uzbekistan.
¹⁶ School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough LE11 3TU, UK.
¹⁷ Department of Genetics and Bioengineering, Faculty of Engineering and Information Technologies, International Burch University, Sarajevo 71000, Bosnia and Herzegovina; Institute for Anthropological Researches, Zagreb, Croatia.
¹⁸ CeGaT GmbH, Tübingen, Praxis für Humangenetik, Tübingen 72076, Germany.
¹⁹ Vinca Institute of Nuclear Sciences, University of Belgrade, M. Petrovica Alasa 12-14, Belgrade 11001, Serbia.
²⁰ Instituto de Pesquisa Rene Rachou, Fundação Oswaldo Cruz, Belo Horizonte, MG 30190-002, Brazil.
²¹ Instituto do Coração, Universidade de São Paulo, São Paulo, SP 05403-900, Brazil.
²² Instituto de Saúde Coletiva, Universidade Federal da Bahia, Salvador, BA 0110-040, Brazil; Center of Data and Knowledge Integration for Health (CIDACS), Fundação Oswaldo Cruz (FIOCRUZ), Salvador, BA 41745-715, Brazil.
²³ Programa de Pós-Graduação em Epidemiologia, Universidade Federal de Pelotas, 464, Pelotas, RS 96001-970, Brazil.
²⁴ Instituto Nacional de Saúde, Distrito de Marracuene, Estrada Nacional N 1, Província de Maputo, Maputo 1120, Mozambique.
²⁵ Department of Genetics & Genome Biology, University of Leicester, Leicester LE1 7RH, UK.
²⁶ National Laboratory of Genomics for Biodiversity (LANGEBIO), CINVESTAV, Irapuato, Guanajuato 36821, Mexico.
²⁷ Department of Human Genetics, KU Leuven, Herestraat 49 - box 602, Leuven 3000, Belgium.
²⁸ Department of Cultural Heritage, University of Bologna, Ravenna Campus, Ravenna 48100, Italy.
²⁹ Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG 31270-901, Brazil.
³⁰ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Biology, University of Padua, Via Ugo Bassi 58B, Padua 35100, Italy.
³¹ Estonian Biocentre, Institute of Genomics, Riia 23, Tartu 51010, Estonia; Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK. Electronic address: francesco.montinaro@gmail.com.

PMID: 31735679
DOI: 10.1016/j.cub.2019.09.076

Abstract

The human genetic diversity of the Americas has been affected by several events of gene flow that have continued since the colonial era and the Atlantic slave trade. Moreover, multiple waves of migration followed by local admixture occurred in the last two centuries, the impact of which has been largely unexplored. Here, we compiled a genome-wide dataset of ∼12,000 individuals from twelve American countries and ∼6,000 individuals from worldwide populations and applied haplotype-based methods to investigate how historical movements from outside the New World affected (1) the genetic structure, (2) the admixture profile, (3) the demographic history, and (4) sex-biased gene-flow dynamics of the Americas. We revealed a high degree of complexity underlying the genetic contribution of European and African populations in North and South America, from both geographic and temporal perspectives, identifying previously unreported sources related to Italy, the Middle East, and to specific regions of Africa.

Keywords: Atlantic Slave Trade; European colonization; admixture history of the Americas; sex-biased admixture.

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The Genomic Impact of European Colonization of the Americas

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The Genomic Impact of European Colonization of the Americas

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