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, 2 (4), e1501385
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Ancient Mitochondrial DNA Provides High-Resolution Time Scale of the Peopling of the Americas

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Ancient Mitochondrial DNA Provides High-Resolution Time Scale of the Peopling of the Americas

Bastien Llamas et al. Sci Adv.

Abstract

The exact timing, route, and process of the initial peopling of the Americas remains uncertain despite much research. Archaeological evidence indicates the presence of humans as far as southern Chile by 14.6 thousand years ago (ka), shortly after the Pleistocene ice sheets blocking access from eastern Beringia began to retreat. Genetic estimates of the timing and route of entry have been constrained by the lack of suitable calibration points and low genetic diversity of Native Americans. We sequenced 92 whole mitochondrial genomes from pre-Columbian South American skeletons dating from 8.6 to 0.5 ka, allowing a detailed, temporally calibrated reconstruction of the peopling of the Americas in a Bayesian coalescent analysis. The data suggest that a small population entered the Americas via a coastal route around 16.0 ka, following previous isolation in eastern Beringia for ~2.4 to 9 thousand years after separation from eastern Siberian populations. Following a rapid movement throughout the Americas, limited gene flow in South America resulted in a marked phylogeographic structure of populations, which persisted through time. All of the ancient mitochondrial lineages detected in this study were absent from modern data sets, suggesting a high extinction rate. To investigate this further, we applied a novel principal components multiple logistic regression test to Bayesian serial coalescent simulations. The analysis supported a scenario in which European colonization caused a substantial loss of pre-Columbian lineages.

Keywords: Ancient DNA; Beringia; Native America; colonization.

Figures

Fig. 1
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
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
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
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).

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