Genetic evidence for two founding populations of the Americas

Abstract

Genetic studies have consistently indicated a single common origin of Native American groups from Central and South America1,2,3,4. However, some morphological studies have suggested a more complex picture, whereby the northeast Asian affinities of present-day Native Americans contrast with a distinctive morphology seen in some of the earliest American skeletons, which share traits with present-day Australasians (indigenous groups in Australia, Melanesia, and island Southeast Asia)5,6,7,8. Here we analyse genome-wide data to show that some Amazonian Native Americans descend partly from a Native American founding population that carried ancestry more closely related to indigenous Australians, New Guineans and Andaman Islanders than to any present-day Eurasians or Native Americans. This signature is not present to the same extent, or at all, in present-day Northern and Central Americans or in a 12,600-year-old Clovis-associated genome, suggesting a more diverse set of founding populations of the Americas than previously accepted.

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Figure 1: South Americans share ancestry with Australasian populations that is not seen in Mesoamericans or North Americans.
Figure 2: A model of population history that can explain the excess affinity to Oceanians observed in Amazonian populations.

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Acknowledgements

We are grateful to the Native American volunteers who contributed the DNA samples used to generate the new data reported in this study and to the Fundação Nacional do Índio (FUNAI, Brazil) for logistical support in sample collection. We thank W. Klitz and C. Winkler for sharing samples for whole-genome sequencing. We thank L. Fehren-Schmitz, Q. Fu, G. Hellenthal, A. Kim, I. Lazaridis, M. Lipson, I. Mathieson, D. Meltzer, P. Moorjani and J. Pickrell for comments and A. Tandon for technical assistance. We thank T. Ferraz and R. Bisso-Machado for assistance with DNA extraction for the genotyping of Brazilian samples. We performed whole-genome sequencing as part of the Simons Genome Diversity Project. Genotyping of the Brazilian samples was performed at the Children’s Hospital of Philadelphia and we particularly thank C. Hou for her support in this. M.C.B., T.H., M.L.P.-E. and F.M.S. were supported by Conselho Nacional do Desenvolvimento Científico e Tecnológico and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brazil). P.S. was supported by the Wenner-Gren foundation and the Swedish Research Council (VR grant 2014-453). D.R. was supported by US National Science Foundation HOMINID grant BCS-1032255, US National Institutes of Health grant GM100233, Simons Foundation Grant 280376 and the Howard Hughes Medical Institute.

Author information

P.S. performed analyses. P.S., S.M., M.C.B., N.C., T.H., M.L.P.-E., F.M.S., N.P. and D.R. prepared datasets. P.S. and D.R. wrote the paper.

Correspondence to Pontus Skoglund or David Reich.

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Competing interests

The authors declare no competing financial interests.

Additional information

Genome sequence data is available from (https://www.simonsfoundation.org/life-sciences/simons-genome-diversity-project-dataset/). New Affymetrix Human Origins array genotype data are available to researchers who send D.R. a signed letter agreeing to respect specific conditions (Supplementary Information section 1).

Extended data figures and tables

Extended Data Figure 1 Clustering analysis.

ADMIXTURE38 clustering analysis performed on the Affymetrix Human Origins data used in this study. To aid in visualization, we only show results for Native American samples and for selected samples from Eurasian populations.

Extended Data Figure 2 qpWave coefficients.

Weights from qpWave for Native American populations and for non-American outgroup populations. No weights are given for Yoruba and Cabecar, as they are used in the computation.

Extended Data Figure 3 Excess allele sharing between the Surui and the Onge.

a, Tests for excess shared derived alleles with the Onge in all possible comparisons of 8 Suruí and 10 Mixe individuals. All Mixe–Suruí comparisons show a positive skew whereas all Mixe–Mixe and Suruí–Suruí comparisons are consistent with 0. Lines correspond to one standard error in either direction. b, Random sequence or genotype errors cannot explain the affinity of the Amazonians to Australasians, as simulated increased errors in the Onge do not cause an increased affinity to Suruí.

Extended Data Figure 4 Signals of admixture as a function of proximity to functional regions.

a, The affinity of 16 Papuan high-coverage genomes to 2 Amazonian Suruí high-coverage genomes as a function of proximity to regions of functional importance (measured by B-value). b, A total of 395 tests of quartets D(Yoruba, X; Y, Z) shows that quartets with significantly positive slopes (|Z| > 3) also yield significant genome-wide D-statistics of the opposite sign. This suggests that signals of admixture are systematically stronger close to functionally important regions.

Extended Data Figure 5 Linkage disequilibrium-based symmetry tests.

a, h4(Yoruba, X; Mixe, Suruí) for SNP pairs within 0.01 cM of each other contrasted with the fraction of SNP pairs in linkage equilibrium in population X (H = 0). Error bars show ± 1 s.e. b, Scatterplot of Z-scores for the f4- and h4-statistics for the same quartets. For both these panels we only use populations with at least 6 samples. c, d, We computed D(Yoruba, X; Y, Z) and h4(Yoruba, X; Y, Z) for many combinations of populations as X, Y and Z using phased Affymetrix Human Origins SNP array data ascertained in a Yoruba individual. Except for Africans who have ancestry from lineages that diverged before the Yoruba used for ascertainment and Oceanians (who have archaic Denisovan ancestry) we observe that |Z| > 3 h4-statistics are always associated with a significantly positive D for the same quartet. e, Correlation of the h4-statistic with the genetic distance separation of pairs of SNPs for h4(Yoruba, X; Mixe, Suruí).

Extended Data Figure 6 Admixture graphs for fitted population history models.

a, An admixture graph where all of Mixe, Suruí and Karitiana are of 100% First American ancestry is rejected with 6 predicted f-statistics at least 3 standard errors from the empirically observed value. b, An admixture graph where the ancestors of Suruí and Karitiana receive 2% ancestry from a lineage related to the Onge is consistent with the data with no outliers. c, An admixture graph where the distinct ancestry in Amazonians is more closely related to Han than to Onge produces 6 outliers. d, An admixture graph with no distinctive ancestry in Karitiana or Suruí but East Asian gene flow into the Mixe produces 7 outliers. e, An admixture graph with no distinctive ancestry in Karitiana or Suruí but MA1-related gene flow into the Mixe produces 6 outliers.

Extended Data Figure 7 Plausible range for the non-First American admixture proportion in Amazonians.

a, Range obtained assuming entirely First American ancestry in the Mixe. b, The maximum proportion of non-First American ancestry in the Mixe that is consistent with the data.

Extended Data Table 1 qpWave analysis provides evidence that Central and South American genetic variation is inconsistent with being derived from a single homogeneous population
Extended Data Table 2 Top 20 D-statistics observed for D(chimpanzee, Old World population; Central Americans, Amazonians)
Extended Data Table 3 f4-statistics for which the statistic predicted by the fitted admixture graphs deviates by more than |Z| > 3 from the statistic computed on the empirical data

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data 1-6, Supplementary Tables and additional references. (PDF 909 kb)

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Skoglund, P., Mallick, S., Bortolini, M. et al. Genetic evidence for two founding populations of the Americas. Nature 525, 104–108 (2015). https://doi.org/10.1038/nature14895

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