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.

INTRODUCTION

The geographic isolation of the Americas delayed human settlement until the end of the Pleistocene [20 to 10 thousand years ago (ka)]; however, despite this relatively recent date, the specific time, place, and route of entry remain uncertain. It is likely that the first peoples moved from Asia across the Bering Land Bridge (1, 2), the landmass between Eurasia and America exposed by lowered sea levels during the Last Glacial Maximum (LGM). However, at this time, much of northern North America was covered by the Cordilleran and Laurentide ice sheets, which blocked access from eastern Beringia (Bering Land Bridge and Alaska/Yukon) southward to the rest of the Americas (Fig. 1A). Shortly after the Cordilleran ice sheet began to retreat ~17 ka (3), a potential Pacific coastal route became available ~15 ka (Fig. 1B) (3, 4), whereas an alternative route through an inland ice-free corridor along the eastern side of the Rocky Mountains opened around ~11.5 to 11 ka (4–6). The timing and route used in the migration event are important in understanding the size, number, and speed of the first migratory wave(s). Timing and route are also pivotal in resolving contentious issues such as the nature of peoples before Clovis—the first widespread archaeologically recognized culture in North America (13.2 to 12.8 ka) (1).

Genetic studies of Native American populations are complicated by the demographic collapse and presumed major loss of genetic diversity following European colonization at the end of the 15th century (7). However, geographically widespread signals of low diversity and shared ancestry (8–13)—particularly striking in maternally inherited mitochondrial and paternally inherited Y-chromosome sequence data—suggest that small founding groups possibly initially entered the Americas in a single migration event that gave rise to most of the ancestry of Native Americans today (9, 12, 14). In contrast, the distribution of some of the rare founding mitochondrial haplogroups (D4h3a along the Pacific coast of North and South America, and X2a in northwestern North America) suggests that distinct migrations along the coastal route and the ice-free corridor occurred within less than 2000 years (15). Recent studies have identified a weak Australasian genomic signature in several Native American groups from the Amazon, compatible with two founding migrations (16), although the Australasian gene flow may have occurred after the initial peopling (17). Irrespective of the number of migration waves, the founding population appears to have rapidly grown and expanded southward (8, 14, 18), with low levels of gene flow between areas following initial dispersion (12, 14).

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It has been suggested that European colonization resulted in a bottleneck in Native American genetic diversity (34, 35). In the present data set, it is notable that no ancient haplotype (Fig. 3B, red lineages) shared a common ancestor with a modern haplotype (Fig. 3B, blue lineages) more recently than ~9.0 ka (Fig. 3B, black triangle in haplogroup A2), despite the number of samples examined from both populations. . . .

As a result, our ancient mitochondrial data suggest that European colonization was followed by local mass mortality and extinction of lineages associated with major population centers of the pre-Columbian past. Our results contrast with previous observations that Native American genetic diversity has been temporally and geographically stable for at least the past 2000 years (33). However, the apparent contradiction between our study and earlier work is likely attributable to a significant improvement of sequence resolution. We also caution that the demographic models tested in this study are likely too simple to encompass the particulars of the colonization of the Americas—despite exploring scenarios with early emergence of geographic structure, as well as ongoing haplotype loss resulting from either serial founder effects and drift, or population displacement and elimination during the expansion of major Central Andean imperial states. Finally, more complete mitochondrial sequence data from early and modern-day populations will be needed to further refine the demographic models. In particular, it will be critical to ensure a strong spatial overlap between archaeological sites and present-day population locations (for example, Peru).

CONCLUSION

The additional resolving power gained from widespread temporal calibrations makes ancient mitochondrial DNA data from South America a very cost-effective approach to examining the precise timing, route, and sequence of events that led to the peopling of the Americas. In addition, this data set provides a genetic view of the possible role played by European colonization in reducing the overall Native American genetic diversity to the low levels observed today. In the absence of archaeological evidence in southern and eastern Beringia that is relevant to the peopling of the Americas, further resolution of the entry and routes of dispersal of the early settlers will be possible with ancient genomic data from South America.