Research ArticleANTHROPOLOGY

Ancient mitochondrial DNA provides high-resolution time scale of the peopling of the Americas

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Science Advances  01 Apr 2016:
Vol. 2, no. 4, e1501385
DOI: 10.1126/sciadv.1501385
  • Fig. 1 Eastern Beringia during the LGM and retreat of the ice sheets.

    (A) Exposed land when sea levels were lowest (light green), modern-day landmass (dark green), and ice sheets (white). At the height of the LGM, the Laurentide and Cordilleran ice sheets blocked access to the Americas from eastern Beringia (that is, the Bering Land Bridge and Alaska/Yukon) (30). Populations west of the Bering Land Bridge were able to migrate southward during the LGM, but those on the Bering Land Bridge were unable to retreat farther than the Aleutian ice belt (arrows). The last point of detectable gene flow between Siberian and Native American ancestral populations (24.9 ka) and the geographic isolation marked by the formation of Native American founder lineages (18.4 ka) are shown (see Fig. 2B for details). The Yana Rhinoceros Horn site (32 ka) and the Swan Point site (14 ka) illustrate the temporal and geographic gaps in the Beringian archaeological record. (B) The ice sheets that began to retreat ~17 ka, opening a potential Pacific coastal route by ~15 ka (arrow). The rapid population expansion (16.0 ka) likely marks the movement south of the ice (see Fig. 3C for details).

  • Fig. 2 Comparison of Bayesian estimates of the TMRCA of the Native American founder haplogroups and of the divergence from Siberian lineages.

    (A) Mean age (symbols) and 95% highest posterior density (HPD) (error bars) for the TMRCA of each of the Native American haplogroups. Shading indicates the period between the oldest lower bound of any 95% HPD and the youngest upper bound of any 95% HPD for each data set. The purple dotted lines show the TMRCA bounds based on tip calibration; the blue dotted lines show the extreme TMRCA bounds from previous publications (26.3 to 9.7 ka) (20, 25). (B) The isolation of Native American populations estimated to have occurred after the last observable divergence between Siberian and Native American lineages (24.9 ka based on the lowest 95% HPD upper bound) and before the oldest date at which all Native American founder haplogroups formed (18.4 ka based on the lowest 95% HPD upper bound). See section S5 for detailed methods.

  • Fig. 3 Dated Bayesian mitogenomic tree and reconstruction of past effective female population size.

    The mitogenomic tree and the demographic plot are based on replicate data set 1, which is representative of the three replicate data sets (fig. S7). (A) Complete tree showing the relationships between the main Native American haplogroups A, B, C, and D, as well as their TMRCA (colored circles). Black circles show the divergences between Siberian and Native American lineages. Siberian clades are shown in black and Native American clades are shown in gray. (B) Detailed tree with Siberian clades (black), modern Native Americans (blue), and ancient Native Americans (red). Colored and black circles as in (A). Gray shadings and empty black circles highlight shared ancestry for individuals from the same geographic location or from the same cultural background. The filled black triangle (haplogroup A2) is the most recent common ancestor between an ancient haplotype and a modern haplotype at ~9 ka. (C) Extended Bayesian skyline plot of female effective population size, based on a generation time of 25 years.

  • Fig. 4 Effects of population structure and European colonization on South American mitochondrial diversity.

    Seven population scenarios simulated with BayeSSC are represented (models A to G). The arrowheads in demographic models C to G represent the time of separation (9 ka) between the population carrying modern haplotypes (Population 0) and the population carrying ancient haplotypes (Population 1) (that is, meta-demes with a pattern of localized small-scale separation across the continent). The bottom-right panel is a PCA plot of summary statistics for the 15,000 simulations for each of the seven models (25% of simulated data are reported; see fig. S10 for the full data set). Observed data from the three replicates are shown as black circles and fall closest to results from model C (green points).

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/2/4/e1501385/DC1

    Supplementary Materials and Methods

    Section S1. Archaeological samples, radiocarbon dating, and DNA contamination control

    Section S2. DNA extraction, library preparation, and mitochondrial capture (ACAD)

    Section S3. DNA extraction and library preparation (UCSC Human Paleogenomics laboratory and HMS Reich laboratory)

    Section S4. Mitochondrial DNA capture (HMS Reich laboratory)

    Section S5. Bayesian phylogenetic analysis of mitochondrial data

    Section S6. Ecological assessment of population sustainability in Beringia

    Section S7. Bayesian coalescent simulations and evaluation of demographic scenarios

    Table S1. Date calibrations for ancient mitogenome sequences.

    Table S2. List of ancient samples, associated metadata, and sequencing results (separate Excel document).

    Table S3. Complete list of accession numbers for modern mitogenome sequences.

    Table S4. Polymerase chain reaction (PCR) primers used for mitochondrial long-range PCR.

    Table S5. Predictive accuracy of the PCMLR model.

    Table S6. Prediction of the population structure model that fits the observed data.

    Table S7. Highest predictive accuracy of the PCMLR model for each population structure model when model C is removed from the analysis.

    Table S8. Prediction of the population structure model that fits the observed data when model C is removed from the analysis.

    Fig. S1. Location of archaeological sites (see table S2 for detailed information about sites and samples).

    Fig. S2. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup A).

    Fig. S3. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup B).

    Fig. S4. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup C).

    Fig. S5. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup D).

    Fig. S6. Maximum parsimony phylogenetic trees of the 93 ancient mitogenomes and three replicate data sets of the 87 modern Native American mitogenomes (see table S3).

    Fig. S7. Extended Bayesian skyline plots of female effective population size for the three replicate data sets.

    Fig. S8. Bayesian estimates of node ages for haplogroups A2, B2, C1, D1, and D4h3a.

    Fig. S9. Results of the date-randomization test for temporal sampling structure.

    Fig. S10. PCA plot of summary statistics for the 15,000 simulations for each of the seven models simulated with BayeSSC (see Fig. 4).

    Fig. S11. PCA plot of summary statistics for the 15,000 simulations for each of the models simulated with BayeSSC, when model C is removed from the PCA.

    References (4886)

  • Supplementary Materials

    This PDF file includes:

    • Supplementary Materials and Methods
    • Section S1. Archaeological samples, radiocarbon dating, and DNA contamination control
    • Section S2. DNA extraction, library preparation, and mitochondrial capture (ACAD)
    • Section S3. DNA extraction and library preparation (UCSC Human Paleogenomics laboratory and HMS Reich laboratory)
    • Section S4. Mitochondrial DNA capture (HMS Reich laboratory)
    • Section S5. Bayesian phylogenetic analysis of mitochondrial data
    • Section S6. Ecological assessment of population sustainability in Beringia
    • Section S7. Bayesian coalescent simulations and evaluation of demographic scenarios
    • Table S1. Date calibrations for ancient mitogenome sequences.
    • Table S2. List of ancient samples, associated metadata, and sequencing results (separate Excel document).
    • Table S3. Complete list of accession numbers for modern mitogenome sequences.
    • Table S4. Polymerase chain reaction (PCR) primers used for mitochondrial long-range PCR.
    • Table S5. Predictive accuracy of the PCMLR model.
    • Table S6. Prediction of the population structure model that fits the observed data.
    • Table S7. Highest predictive accuracy of the PCMLR model for each population structure model when model C is removed from the analysis.
    • Table S8. Prediction of the population structure model that fits the observed data when model C is removed from the analysis.
    • Fig. S1. Location of archaeological sites (see table S2 for detailed information about sites and samples).
    • Fig. S2. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup A).
    • Fig. S3. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup B).
    • Fig. S4. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup C).
    • Fig. S5. Phylogenetic tree of newly sequenced ancient mitogenomes (haplogroup D).
    • Fig. S6. Maximum parsimony phylogenetic trees of the 93 ancient mitogenomes and three replicate data sets of the 87 modern Native American mitogenomes (see table S3).
    • Fig. S7. Extended Bayesian skyline plots of female effective population size for the three replicate data sets.
    • Fig. S8. Bayesian estimates of node ages for haplogroups A2, B2, C1, D1, and D4h3a.
    • Fig. S9. Results of the date-randomization test for temporal sampling structure.
    • Fig. S10. PCA plot of summary statistics for the 15,000 simulations for each of the seven models simulated with BayeSSC (see Fig. 4).
    • Fig. S11. PCA plot of summary statistics for the 15,000 simulations for each of the models simulated with BayeSSC, when model C is removed from the PCA.
    • References (48–86)

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    Other Supplementary Material for this manuscript includes the following:

    • Table S2. List of ancient samples, associated metadata, and sequencing results (separate Excel document

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