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Disentangling Signatures of Selection Before and After European Colonization in Latin Americans

Authors
  • Mendoza-Revilla, Javier1, 2, 3
  • Chacón-Duque, J. Camilo4, 5
  • Fuentes-Guajardo, Macarena6
  • Ormond, Louise1
  • Wang, Ke1, 7
  • Hurtado, Malena3
  • Villegas, Valeria3
  • Granja, Vanessa3
  • Acuña-Alonzo, Victor8
  • Jaramillo, Claudia9
  • Arias, William9
  • Barquera, Rodrigo7, 8
  • Gómez-Valdés, Jorge8
  • Villamil-Ramírez, Hugo10, 11
  • Silva de Cerqueira, Caio C.12
  • Badillo Rivera, Keyla M.13
  • Nieves-Colón, Maria A.14
  • Gignoux, Christopher R.15
  • Wojcik, Genevieve L.16
  • Moreno-Estrada, Andrés17
  • And 15 more
  • 1 Department of Genetics, Evolution and Environment, and UCL Genetics Institute, University College London, United Kingdom , (United Kingdom)
  • 2 Human Evolutionary Genetics Unit, Institut Pasteur, UMR2000, CNRS, France , (France)
  • 3 Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, Perú , (Peru)
  • 4 Centre for Palaeogenetics, Sweden , (Sweden)
  • 5 Department of Archaeology and Classical Studies, Stockholm University, Sweden , (Sweden)
  • 6 Departamento de Tecnología Médica, Facultad de Ciencias de la Salud, Universidad de Tarapacá, Chile , (Chile)
  • 7 Department of Archaeogenetics, Max Planck Institute for Evolutionary Anthropology, Germany , (Germany)
  • 8 National School of Anthropology and History, Mexico , (Mexico)
  • 9 GENMOL (Genética Molecular), Universidad de Antioquia, Colombia , (Colombia)
  • 10 Unidad de Genómica de Poblaciones Aplicada a la Salud, Facultad de Química, UNAM-Instituto Nacional de Medicina Genómica, Mexico , (Mexico)
  • 11 Universidad Nacional Autónoma de México e Instituto Nacional de Medicina Genómica, Mexico , (Mexico)
  • 12 Departamento de Genética, Universidade Federal do Rio Grande do Sul, Brazil , (Brazil)
  • 13 Department of Genetics, Stanford School of Medicine, USA , (United States)
  • 14 Department of Anthropology, University of Minnesota Twin Cities, USA , (United States)
  • 15 Department of Biostatistics and Informatics, University of Colorado Anschutz Medical Campus, USA , (United States)
  • 16 Bloomberg School of Public Health, John Hopkins University, USA , (United States)
  • 17 Laboratorio Nacional de Genómica para la Biodiversidad (UGA-LANGEBIO), CINVESTAV, Mexico , (Mexico)
  • 18 University of São Paulo
  • 19 Instituto Patagónico de Ciencias Sociales y Humanas-Centro Nacional Patagónico, CONICET, Argentina , (Argentina)
  • 20 Instituto de Alta Investigación, Universidad de Tarapacá, Chile , (Chile)
  • 21 Schools of BioSciences and Mathematics & Statistics, University of Melbourne, Australia , (Australia)
  • 22 School of Biological and Behavioural Sciences, Queen Mary University of London, United Kingdom , (United Kingdom)
  • 23 School of Mathematics and Statistics, Faculty of Science, Technology, Engineering and Mathematics, The Open University, United Kingdom , (United Kingdom)
  • 24 Ministry of Education Key Laboratory of Contemporary Anthropology and Collaborative Innovation Center of Genetics and Development, Fudan University, China , (China)
  • 25 Aix-Marseille Université, CNRS, EFS, ADES, France , (France)
Type
Published Article
Journal
Molecular Biology and Evolution
Publisher
Oxford University Press
Publication Date
Apr 19, 2022
Volume
39
Issue
4
Identifiers
DOI: 10.1093/molbev/msac076
PMID: 35460423
PMCID: PMC9034689
Source
PubMed Central
Keywords
Disciplines
  • AcademicSubjects/SCI01130
  • AcademicSubjects/SCI01180
License
Unknown

Abstract

Throughout human evolutionary history, large-scale migrations have led to intermixing (i.e., admixture) between previously separated human groups. Although classical and recent work have shown that studying admixture can yield novel historical insights, the extent to which this process contributed to adaptation remains underexplored. Here, we introduce a novel statistical model, specific to admixed populations, that identifies loci under selection while determining whether the selection likely occurred post-admixture or prior to admixture in one of the ancestral source populations. Through extensive simulations, we show that this method is able to detect selection, even in recently formed admixed populations, and to accurately differentiate between selection occurring in the ancestral or admixed population. We apply this method to genome-wide SNP data of ∼4,000 individuals in five admixed Latin American cohorts from Brazil, Chile, Colombia, Mexico, and Peru. Our approach replicates previous reports of selection in the human leukocyte antigen region that are consistent with selection post-admixture. We also report novel signals of selection in genomic regions spanning 47 genes, reinforcing many of these signals with an alternative, commonly used local-ancestry-inference approach. These signals include several genes involved in immunity, which may reflect responses to endemic pathogens of the Americas and to the challenge of infectious disease brought by European contact. In addition, some of the strongest signals inferred to be under selection in the Native American ancestral groups of modern Latin Americans overlap with genes implicated in energy metabolism phenotypes, plausibly reflecting adaptations to novel dietary sources available in the Americas.

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