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Research Article

Comparing signals of natural selection between three Indigenous North American populations

Austin W. Reynolds, Jaime Mata-Míguez, Aida Miró-Herrans, Marcus Briggs-Cloud, Ana Sylestine, Francisco Barajas-Olmos, View ORCID ProfileHumberto Garcia-Ortiz, Margarita Rzhetskaya, Lorena Orozco, Jennifer A. Raff, M. Geoffrey Hayes, and Deborah A. Bolnick
  1. aDepartment of Anthropology, University of California, Davis, CA 95616;
  2. bDepartment of Anthropology, The University of Texas at Austin, Austin, TX 78712;
  3. cFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611;
  4. dMaskoke, Gainesville, FL 32611;
  5. eSchool of Natural Resources and Environment, University of Florida, Gainesville, FL 32611;
  6. fCoushatta Tribe of Louisiana, Elton, LA 70532;
  7. gNational Institute of Genomic Medicine, Delegación Tlalpan, 14610 México;
  8. hDivision of Endocrinology, Metabolism, and Molecular Medicine, Department of Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611;
  9. iDepartment of Anthropology, University of Kansas, Lawrence, KS 66045-7556;
  10. jCenter for Genetic Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611;
  11. kDepartment of Anthropology, Northwestern University, Evanston, IL 60208;
  12. lDepartment of Anthropology, University of Connecticut, Storrs, CT 06269-1176;
  13. mInstitute for Systems Genomics, University of Connecticut, Storrs, CT 06269-1176

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PNAS May 7, 2019 116 (19) 9312-9317; first published April 15, 2019; https://doi.org/10.1073/pnas.1819467116
Austin W. Reynolds
aDepartment of Anthropology, University of California, Davis, CA 95616;
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  • For correspondence: awreynolds@ucdavis.edu
Jaime Mata-Míguez
bDepartment of Anthropology, The University of Texas at Austin, Austin, TX 78712;
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Aida Miró-Herrans
cFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611;
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Marcus Briggs-Cloud
dMaskoke, Gainesville, FL 32611;
eSchool of Natural Resources and Environment, University of Florida, Gainesville, FL 32611;
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Ana Sylestine
fCoushatta Tribe of Louisiana, Elton, LA 70532;
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Francisco Barajas-Olmos
gNational Institute of Genomic Medicine, Delegación Tlalpan, 14610 México;
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Humberto Garcia-Ortiz
gNational Institute of Genomic Medicine, Delegación Tlalpan, 14610 México;
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  • ORCID record for Humberto Garcia-Ortiz
Margarita Rzhetskaya
hDivision of Endocrinology, Metabolism, and Molecular Medicine, Department of Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611;
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Lorena Orozco
gNational Institute of Genomic Medicine, Delegación Tlalpan, 14610 México;
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Jennifer A. Raff
iDepartment of Anthropology, University of Kansas, Lawrence, KS 66045-7556;
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M. Geoffrey Hayes
hDivision of Endocrinology, Metabolism, and Molecular Medicine, Department of Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611;
jCenter for Genetic Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL 60611;
kDepartment of Anthropology, Northwestern University, Evanston, IL 60208;
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Deborah A. Bolnick
lDepartment of Anthropology, University of Connecticut, Storrs, CT 06269-1176;
mInstitute for Systems Genomics, University of Connecticut, Storrs, CT 06269-1176
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  1. Edited by Anne C. Stone, Arizona State University, Tempe, AZ, and approved March 8, 2019 (received for review November 13, 2018)

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Significance

Recent studies have shown that humans have adapted to many different environments around the world. However, few studies have centered on Indigenous groups in the Americas. We present a comparative analysis of genetic adaptations in humans across North America using genome-wide scans for signals of natural selection in three populations inhabiting vastly different environments. We find evidence for adaptation to cold and high latitudes in an Alaskan population, whereas infectious disease was a strong selective pressure in the southeastern United States and central Mexico. Because there are few shared signals of selection between populations, these sweeps likely occurred after population differentiation in the Americas. This study fills an important gap in our knowledge of genetic adaptations in humans.

Abstract

While many studies have highlighted human adaptations to diverse environments worldwide, genomic studies of natural selection in Indigenous populations in the Americas have been absent from this literature until very recently. Since humans first entered the Americas some 20,000 years ago, they have settled in many new environments across the continent. This diversity of environments has placed variable selective pressures on the populations living in each region, but the effects of these pressures have not been extensively studied to date. To help fill this gap, we collected genome-wide data from three Indigenous North American populations from different geographic regions of the continent (Alaska, southeastern United States, and central Mexico). We identified signals of natural selection in each population and compared signals across populations to explore the differences in selective pressures among the three regions sampled. We find evidence of adaptation to cold and high-latitude environments in Alaska, while in the southeastern United States and central Mexico, pathogenic environments seem to have created important selective pressures. This study lays the foundation for additional functional and phenotypic work on possible adaptations to varied environments during the history of population diversification in the Americas.

  • population genomics
  • natural selection
  • Native Americans
  • Alaskan Natives
  • human evolutionary genetics

Footnotes

  • ↵1To whom correspondence should be addressed. Email: awreynolds{at}ucdavis.edu.
  • Author contributions: A.W.R. and D.A.B. designed research; A.W.R., J.M.-M., A.M.-H., M.B.-C., A.S., M.R., J.A.R., and M.G.H. performed research; A.W.R., F.B.-O., H.G.-O., and L.O. analyzed data; and A.W.R. and D.A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1819467116/-/DCSupplemental.

Published under the PNAS license.

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Comparing signals of natural selection between three Indigenous North American populations
Austin W. Reynolds, Jaime Mata-Míguez, Aida Miró-Herrans, Marcus Briggs-Cloud, Ana Sylestine, Francisco Barajas-Olmos, Humberto Garcia-Ortiz, Margarita Rzhetskaya, Lorena Orozco, Jennifer A. Raff, M. Geoffrey Hayes, Deborah A. Bolnick
Proceedings of the National Academy of Sciences May 2019, 116 (19) 9312-9317; DOI: 10.1073/pnas.1819467116

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Comparing signals of natural selection between three Indigenous North American populations
Austin W. Reynolds, Jaime Mata-Míguez, Aida Miró-Herrans, Marcus Briggs-Cloud, Ana Sylestine, Francisco Barajas-Olmos, Humberto Garcia-Ortiz, Margarita Rzhetskaya, Lorena Orozco, Jennifer A. Raff, M. Geoffrey Hayes, Deborah A. Bolnick
Proceedings of the National Academy of Sciences May 2019, 116 (19) 9312-9317; DOI: 10.1073/pnas.1819467116
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Proceedings of the National Academy of Sciences: 116 (19)
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