A genomic view of the peopling of the Americas

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Whole-genome studies have documented that most Native American ancestry stems from a single population that diversified within the continent more than twelve thousand years ago. However, this shared ancestry hides a more complex history whereby at least four distinct streams of Eurasian migration have contributed to present-day and prehistoric Native American populations. Whole genome studies enhanced by technological breakthroughs in ancient DNA now provide evidence of a sequence of events involving initial migrations from a structured Northeast Asian source population with differential relatedness to present-day Australasian populations, followed by a divergence into northern and southern Native American lineages. During the Holocene, new migrations from Asia introduced the Saqqaq/Dorset Paleoeskimo population to the North American Arctic ∼4500 years ago, ancestry that is potentially connected with ancestry found in Athabaskan-speakers today. This was then followed by a major new population turnover in the high Arctic involving Thule-related peoples who are the ancestors of present-day Inuit. We highlight several open questions that could be addressed through future genomic research.

Introduction

The peopling of the Americas represented the culmination of a Late Pleistocene expansion of anatomically modern humans out of Africa. Archaeological evidence indicates that groups subsisting on hunting lived in extreme northeast Siberia (71° N) by at least 28,000 years ago [1]. Human groups adapted to the mammoth steppe habitat were thus poised to enter Beringia  the landmass between Alaska and Eurasia that is now submerged  by this time [2, 3]. The path from Beringia to the more temperate parts of the American continents, however, was blocked by the merged Laurentide and Cordilleran ice sheets that covered northern North America until the end of the Last Glacial Maximum. The ice retreated from parts of the Pacific coast ∼16,000 years ago, raising the possibility of a coastal migration after this time, and within a few thousand years a habitable corridor through the center of the continent opened between the two ice sheets [4]. The first unambiguous evidence of modern humans in the Americas dates to between 14,000 and 15,000 years ago [5, 6, 7, 8], and was likely the consequence of migration from Beringia.

Major debates about the peopling of the Americas have focused on the question of whether the first early human populations in the Americas are directly ancestral to present-day Native Americans, as well as on the number, mode, and timing of secondary migrations to the Americas. Advances in genomics have, within the last five years, enabled the collection of far more data from present-day Native Americans than were available previously, and have also made it possible for the first time to access DNA from ancient Native American remains. Analysis of these data has highlighted a minimum of four distinct streams of Asian ancestry, some of which were not clear from the archaeological evidence. We review the contributions of genomic data to understanding the prehistory of the Americas, and outline outstanding questions where it may be able to provide additional insight.

Section snippets

The power of the whole genome

The first meaningful genetic insights about Native American population history came from mitochondrial DNA, a segment of about 16,500 base pairs (approximately 1/200,000th of the genome) that is passed exclusively along the maternal line. Mitochondrial DNA was one of the first parts of the genome to be heavily investigated to learn about human population history for several reasons. First, it is highly variable on a per-nucleotide level and thus sequencing only a short stretch can detect

Sources of Native American ancestry

Under the hypothesis that Native American ancestry stems from a single founder population that separated earlier from Eurasian populations, differences in allele frequencies between Native American groups should have developed independently from Eurasian allele frequencies. This simple null hypothesis makes it possible to explicitly test hypotheses about the number of American founder populations. Reich et al. [23••] applied this idea to the first comprehensive genome-wide data from Native

The main ancestral stream giving rise to Native American ancestry

One of the most important pieces of genetic evidence relevant to the peopling of the Americas was the sequencing of a genome from the remains of a child (‘Anzick-1’) buried with Clovis artifacts in western Montana and directly dated to 12,600 before present (BP) [25••]. This child was consistent with deriving all of his ancestry from the same founding population as Central and South Americans (Figure 1), contradicting the ‘Solutrean hypothesis’ of transatlantic migration from Upper Paleolithic

Major admixture during the formation of the ancestral population of Native Americans

Until 2014, efforts to infer demographic parameters for the peopling of the New World based on genetic data focused on modeling Native Americans as an offshoot of East Asian ancestry [17, 20, 23••, 29, 30, 31, 32, 33, 34•]. However, the analysis of the genome of a 24,000 year-old individual from the Mal’ta site near Lake Baikal in Central Siberia revealed that this model is untenable. The Mal’ta individual shared genetic affinities to both European (West Eurasian) and Native American

An Australasian connection

Recently, we carried out a stringent test of the null hypothesis of a single founding population of Central and South Americans using genome-wide data from diverse Native Americans [36••]. We detected a statistically clear signal linking Native Americans in the Amazonian region of Brazil to present-day Australo-Melanesians and Andaman Islanders (‘Australasians’). Specifically, we found that Australasians share significantly more genetic variants with some Amazonian populations  including ones

Post-glacial migrations into North America

The archaeological record of the North American Arctic documents a transformation beginning around a thousand years ago and associated with the Thule cultural complex. The Thule culture advanced into a North American Arctic occupied by the descendants of previous migrations (Figure 3), referred to as Paleoeskimos and culturally represented by the Saqqaq and Dorset technological complexes [41]. Genome-wide data from a ∼4000 year old Saqqaq culture individual in Greenland  the first genome-wide

Prospects

Far more remains to learn about the genomic history of Native Americans than has already been discovered. Major directions for future data collection include more ancient DNA data, and filling in sampling gaps of present-day Native American populations, especially in the United States. We conclude by highlighting five major open questions about Native American population history that we believe may be meaningfully addressed using genomic data in the coming years.

  • (1)

    What is the origin of Population

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Lars Fehren-Schmitz, David Meltzer and Jennifer Raff for critical comments. PS was supported by the Wenner-Gren foundation and the Swedish Research Council (VR grant 2014-453). DR was supported by NIH grant GM100233, by NSF HOMINID BCS-1032255, and is a Howard Hughes Medical Institute investigator.

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