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Research Article

Genetic signature of natural selection in first Americans

Carlos Eduardo G. Amorim, Kelly Nunes, Diogo Meyer, David Comas, Maria Cátira Bortolini, Francisco Mauro Salzano, and Tábita Hünemeier
  1. aDepartment of Biological Sciences, Columbia University, New York, NY 10027;
  2. bDepartmento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, 03178-200 São Paulo, Brazil;
  3. cInstitut de Biologia Evolutiva, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, 08003 Barcelona, Spain;
  4. dDepartamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 Porto Alegre, Brazil

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PNAS February 28, 2017 114 (9) 2195-2199; first published February 13, 2017; https://doi.org/10.1073/pnas.1620541114
Carlos Eduardo G. Amorim
aDepartment of Biological Sciences, Columbia University, New York, NY 10027;
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Kelly Nunes
bDepartmento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, 03178-200 São Paulo, Brazil;
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Diogo Meyer
bDepartmento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, 03178-200 São Paulo, Brazil;
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David Comas
cInstitut de Biologia Evolutiva, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, 08003 Barcelona, Spain;
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Maria Cátira Bortolini
dDepartamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 Porto Alegre, Brazil
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Francisco Mauro Salzano
dDepartamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, 91501-970 Porto Alegre, Brazil
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  • For correspondence: francisco.salzano@ufrgs.br hunemeier@usp.br
Tábita Hünemeier
bDepartmento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, 03178-200 São Paulo, Brazil;
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  • For correspondence: francisco.salzano@ufrgs.br hunemeier@usp.br
  1. Contributed by Francisco Mauro Salzano, January 2, 2017 (sent for review July 5, 2016; reviewed by Theodore G. Schurr and Anne C. Stone)

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Significance

There is much interest in understanding the role of natural selection in shaping physiological adaptations to climate, diet, and diseases in humans. We investigated this issue by analyzing genomic data from Native American populations inhabiting different ecological regions and ancient Native Americans. We found signals of natural selection at the fatty acid desaturases (FADS) genes not only in an Arctic population, as was previously found, but throughout the Americas, suggesting a single and strong adaptive event that occurred in Beringia, before the range expansion of the first Americans within the American continent and Greenland.

Abstract

When humans moved from Asia toward the Americas over 18,000 y ago and eventually peopled the New World they encountered a new environment with extreme climate conditions and distinct dietary resources. These environmental and dietary pressures may have led to instances of genetic adaptation with the potential to influence the phenotypic variation in extant Native American populations. An example of such an event is the evolution of the fatty acid desaturases (FADS) genes, which have been claimed to harbor signals of positive selection in Inuit populations due to adaptation to the cold Greenland Arctic climate and to a protein-rich diet. Because there was evidence of intercontinental variation in this genetic region, with indications of positive selection for its variants, we decided to compare the Inuit findings with other Native American data. Here, we use several lines of evidence to show that the signal of FADS-positive selection is not restricted to the Arctic but instead is broadly observed throughout the Americas. The shared signature of selection among populations living in such a diverse range of environments is likely due to a single and strong instance of local adaptation that took place in the common ancestral population before their entrance into the New World. These first Americans peopled the whole continent and spread this adaptive variant across a diverse set of environments.

  • peopling of America
  • natural selection
  • genetics
  • first Americans

Footnotes

  • ↵1C.E.G.A. and K.N. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: francisco.salzano{at}ufrgs.br or hunemeier{at}usp.br.
  • Author contributions: C.E.G.A., K.N., and T.H. designed research; C.E.G.A., K.N., and T.H. performed research; C.E.G.A., K.N., and T.H. analyzed data; and C.E.G.A., K.N., D.M., D.C., M.C.B., F.M.S., and T.H. wrote the paper.

  • Reviewers: T.G.S., University of Pennsylvania; and A.C.S., Arizona State University.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1620541114/-/DCSupplemental.

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Natural selection in first Americans
Carlos Eduardo G. Amorim, Kelly Nunes, Diogo Meyer, David Comas, Maria Cátira Bortolini, Francisco Mauro Salzano, Tábita Hünemeier
Proceedings of the National Academy of Sciences Feb 2017, 114 (9) 2195-2199; DOI: 10.1073/pnas.1620541114

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Natural selection in first Americans
Carlos Eduardo G. Amorim, Kelly Nunes, Diogo Meyer, David Comas, Maria Cátira Bortolini, Francisco Mauro Salzano, Tábita Hünemeier
Proceedings of the National Academy of Sciences Feb 2017, 114 (9) 2195-2199; DOI: 10.1073/pnas.1620541114
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Proceedings of the National Academy of Sciences: 114 (9)
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