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Genome Biol. 2020 Feb 7;21(1):29. doi: 10.1186/s13059-020-1946-2.

Admixture-enabled selection for rapid adaptive evolution in the Americas.

Author information

1
School of Biological Sciences, Georgia Institute of Technology, 950 Atlantic Drive, Atlanta, GA, 30332, USA.
2
IHRC-Georgia Tech Applied Bioinformatics Laboratory, Atlanta, GA, USA.
3
PanAmerican Bioinformatics Institute, Cali, Valle del Cauca, Colombia.
4
Department of Genetics, University of Georgia, Athens, GA, USA.
5
Institute of Bioinformatics, University of Georgia, Athens, GA, USA.
6
Biomedical Research Institute (COL0082529), Cali, Colombia.
7
Universidad Santiago de Cali, Cali, Colombia.
8
School of Biological Sciences, Georgia Institute of Technology, 950 Atlantic Drive, Atlanta, GA, 30332, USA. king.jordan@biology.gatech.edu.
9
IHRC-Georgia Tech Applied Bioinformatics Laboratory, Atlanta, GA, USA. king.jordan@biology.gatech.edu.
10
PanAmerican Bioinformatics Institute, Cali, Valle del Cauca, Colombia. king.jordan@biology.gatech.edu.

Abstract

BACKGROUND:

Admixture occurs when previously isolated populations come together and exchange genetic material. We hypothesize that admixture can enable rapid adaptive evolution in human populations by introducing novel genetic variants (haplotypes) at intermediate frequencies, and we test this hypothesis through the analysis of whole genome sequences sampled from admixed Latin American populations in Colombia, Mexico, Peru, and Puerto Rico.

RESULTS:

Our screen for admixture-enabled selection relies on the identification of loci that contain more or less ancestry from a given source population than would be expected given the genome-wide ancestry frequencies. We employ a combined evidence approach to evaluate levels of ancestry enrichment at single loci across multiple populations and multiple loci that function together to encode polygenic traits. We find cross-population signals of African ancestry enrichment at the major histocompatibility locus on chromosome 6, consistent with admixture-enabled selection for enhanced adaptive immune response. Several of the human leukocyte antigen genes at this locus, such as HLA-A, HLA-DRB51, and HLA-DRB5, show independent evidence of positive selection prior to admixture, based on extended haplotype homozygosity in African populations. A number of traits related to inflammation, blood metabolites, and both the innate and adaptive immune system show evidence of admixture-enabled polygenic selection in Latin American populations.

CONCLUSIONS:

The results reported here, considered together with the ubiquity of admixture in human evolution, suggest that admixture serves as a fundamental mechanism that drives rapid adaptive evolution in human populations.

KEYWORDS:

Admixture; Genetic ancestry; Polygenic traits; Population genomics; Positive selection; Rapid adaptive evolution

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