Beringian standstill and spread of Native American founders.
ABSTRACT Native Americans derive from a small number of Asian founders who likely arrived to the Americas via Beringia. However, additional details about the initial colonization of the Americas remain unclear. To investigate the pioneering phase in the Americas we analyzed a total of 623 complete mtDNAs from the Americas and Asia, including 20 new complete mtDNAs from the Americas and seven from Asia. This sequence data was used to direct high-resolution genotyping from 20 American and 26 Asian populations. Here we describe more genetic diversity within the founder population than was previously reported. The newly resolved phylogenetic structure suggests that ancestors of Native Americans paused when they reached Beringia, during which time New World founder lineages differentiated from their Asian sister-clades. This pause in movement was followed by a swift migration southward that distributed the founder types all the way to South America. The data also suggest more recent bi-directional gene flow between Siberia and the North American Arctic.
- SourceAvailable from: Theodore Schurr[show abstract] [hide abstract]
ABSTRACT: The mtDNA variation of 321 individuals from 17 Native American populations was examined by high-resolution restriction endonuclease analysis. All mtDNAs were amplified from a variety of sources by using PCR. The mtDNA of a subset of 38 of these individuals was also analyzed by D-loop sequencing. The resulting data were combined with previous mtDNA data from five other Native American tribes, as well as with data from a variety of Asian populations, and were used to deduce the phylogenetic relationships between mtDNAs and to estimate sequence divergences. This analysis revealed the presence of four haplotype groups (haplogroups A, B, C, and D) in the Amerind, but only one haplogroup (A) in the Na-Dene, and confirmed the independent origins of the Amerinds and the Na-Dene. Further, each haplogroup appeared to have been founded by a single mtDNA haplotype, a result which is consistent with a hypothesized founder effect. Most of the variation within haplogroups was tribal specific, that is, it occurred as tribal private polymorphisms. These observations suggest that the process of tribalization began early in the history of the Amerinds, with relatively little intertribal genetic exchange occurring subsequently. The sequencing of 341 nucleotides in the mtDNA D-loop revealed that the D-loop sequence variation correlated strongly with the four haplogroups defined by restriction analysis, and it indicated that the D-loop variation, like the haplotype variation, arose predominantly after the migration of the ancestral Amerinds across the Bering land bridge.The American Journal of Human Genetics 10/1993; 53(3):563-90. · 11.20 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: The mitochondrial DNA (mtDNA) sequence variation of the South American Ticuna, the Central American Maya, and the North American Pima was analyzed by restriction-endonuclease digestion and oligonucleotide hybridization. The analysis revealed that Amerindian populations have high frequencies of mtDNAs containing the rare Asian RFLP HincII morph 6, a rare HaeIII site gain, and a unique AluI site gain. In addition, the Asian-specific deletion between the cytochrome c oxidase subunit II (COII) and tRNA(Lys) genes was also prevalent in both the Pima and the Maya. These data suggest that Amerindian mtDNAs derived from at least four primary maternal lineages, that new tribal-specific variants accumulated as these mtDNAs became distributed throughout the Americas, and that some genetic variation may have been lost when the progenitors of the Ticuna separated from the North and Central American populations.The American Journal of Human Genetics 04/1990; 46(3):613-23. · 11.20 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: The timing and number of prehistoric migrations involved in the settlement of the American continent is subject to intense debate. Here, we reanalyze Native American control region mtDNA data and demonstrate that only an appropriate phylogenetic analysis accompanied by an appreciation of demographic factors allows us to discern different migrations and to estimate their ages. Reappraising 574 mtDNA control region sequences from aboriginal Siberians and Native Americans, we confirm in agreement with linguistic, archaeological and climatic evidence that (i) the major wave of migration brought one population, ancestral to the Amerinds, from northeastern Siberia to America 20,000-25,000 years ago and (ii) a rapid expansion of a Beringian source population took place at the end of the Younger Dryas glacial phase approximately 11,300 years ago, ancestral to present Eskimo and Na-Dene populations.The American Journal of Human Genetics 11/1996; 59(4):935-45. · 11.20 Impact Factor
Beringian Standstill and Spread of Native American
Erika Tamm1, Toomas Kivisild1,2, Maere Reidla1, Mait Metspalu1, David Glenn Smith3, Connie J. Mulligan4, Claudio M. Bravi5, Olga Rickards6,
Cristina Martinez-Labarga6, Elsa K. Khusnutdinova7, Sardana A. Fedorova1,8, Maria V. Golubenko1,9, Vadim A. Stepanov9, Marina A. Gubina10,
Sergey I. Zhadanov1,10,11, Ludmila P. Ossipova10, Larisa Damba1,10, Mikhail I. Voevoda10, Jose E. Dipierri12, Richard Villems1, Ripan S. Malhi13*
1Department of Evolutionary Biology, University of Tartu, Estonian Biocentre, Tartu, Estonia, 2Leverhulme Centre for Human Evolutionary Studies,
University of Cambridge, Cambridge, United Kingdom, 3Department of Anthropology, University of California at Davis, Davis, California, United
States of America, 4Department of Anthropology, University of Florida, Gainesville, Florida, United States of America, 5Instituto Multidisciplinario de
Biologı ´a Celular, La Plata, Argentina, 6Department of Biology, University of Rome Tor Vergata, Rome, Italy, 7Institute of Biochemistry and Genetics,
Ufa Research Center, Russian Academy of Sciences, Ufa, Russia, 8Department of Molecular Genetics, Yakut Research Center, Russian Academy of
Medical Sciences, Yakutia, Russia, 9Institute of Medical Genetics, Tomsk Research Center, Russian Academy of Medical Sciences, Tomsk, Russia,
10Institute of Genetics and Cytology, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia, 11Department of Anthropology,
University of Pennsylvania, Philadelphia, Pennsylvania, United States of America, 12Instituto de Biologia de la Altura–Universidad Nacional de Jujuy,
Jujuy, Argentina, 13Department of Anthropology, Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Champaign, Illinois,
United States of America
Native Americans derive from a small number of Asian founders who likely arrived to the Americas via Beringia. However,
additional details about the intial colonization of the Americas remain unclear. To investigate the pioneering phase in the
Americas we analyzed a total of 623 complete mtDNAs from the Americas and Asia, including 20 new complete mtDNAs from
the Americas and seven from Asia. This sequence data was used to direct high-resolution genotyping from 20 American and 26
Asian populations. Here we describe more genetic diversity within the founder population than was previously reported. The
newly resolved phylogenetic structure suggests that ancestors of Native Americans paused when they reached Beringia,
during which time New World founder lineages differentiated from their Asian sister-clades. This pause in movement was
followed by a swift migration southward that distributed the founder types all the way to South America. The data also
suggest more recent bi-directional gene flow between Siberia and the North American Arctic.
Citation: Tamm E, Kivisild T, Reidla M, Metspalu M, Smith DG, et al (2007) Beringian Standstill and Spread of Native American Founders. PLoS ONE 2(9):
The mitochondrial DNA haplogroup nomenclature that is widely
used today in population and medical genetics, forensic science,
and in other interdisciplinary studies, traces back to the analysis of
Native American populations by Torroni et al. ,. The first
four letters of the phylogenetic alphabet for mtDNA haplogroups -
A-D - were coined to refer to just four founding haplogroups that
exhibit virtually all North and South American mtDNA diversity.
Genetic studies demonstrate that Native Americans inherited
their mitochondrial DNA (mtDNA) from a handful of founders
who arrived from Asia via Beringia ,. No more than four
major pan American and three minor North American founding
mtDNA haplotypes (A2, B2, C1, D1 and X2a, D2, D3,
respectively) have been convincingly established in previous studies
of control region sequence, RFLP markers and 30 complete
mtDNA genomes (Table 1) [1–14]. The paucity of established
founding mtDNAs suggests that the number of migrants that
initially peopled the Americas was relatively low. However,
determining the full range of diversity surviving to the present
day in the founding population requires high-resolution mtDNA
sequence data. Previous estimates of mtDNA diversity are
predominantly based on control region sequences representing
only a minor fraction of the mtDNA genome. In addition, control
region sequences experience a high frequency of recurrent
mutations, potentially obscuring the identification of additional
founding mtDNAs [14–19].
Even though some additional minor founder types have been
later identified in North America, such as X, the hypothesis of just
four major founder types in the initial colonization of the New
World remains uncontested. However, the timing of their entry
remains debated. Previous studies of mtDNA data place estimates
for the peopling of the New World in a broad range from 11,000
to over 40,000 years before present (ybp) [reviewed by 20],
although more recent estimates range from 20,000–15,000 ybp
. Recent archaeological evidence places Homo sapiens in
northeastern Siberia at the Yana Rhinoceros Horn Site as early
as 30,000 ybp  about twice the 15,000 ybp  date for
humans at the southern end of South America. These archaeo-
logical dates suggest two likely scenarios. First, the ancestors of
Native Americans peopled Beringia before the Last Glacial
Maximum, but remained locally isolated (likely due to ecological
barriers) until entering the Americas at 15,000 ybp (Beringian
incubation model, BIM) . Second, the ancestors of Native
Americans did not reach Beringia until just before 15,000 ybp,
and then moved continuously on into the Americas, being recently
derived from a larger parent Asian population (direct colonization
Academic Editor: Dee Carter, University of Sydney, Australia
Received April 24, 2007; Accepted August 10, 2007; Published September 5,
Copyright: ? 2007 Tamm et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited.
Funding: Funding for this work is from NSF BCS#0422144 to RSM and from the
University of Tartu #PBGMR06901 to TK.
Competing Interests: The authors have declared that no competing interests
* To whom correspondence should be addressed. E-mail: firstname.lastname@example.org
PLoS ONE | www.plosone.org1September 2007 | Issue 9 | e829
The DCM model hypothesizes the presence of founding
mtDNA haplotypes that include members from both Northeast
Asia and the Americas. It presumes a continuous movement of
recently derived migrants across Beringia. In contrast, the BIM
model predicts widespread, derived founding haplotypes specific to
the Americas that are not found in Asia. This implies that migrants
were isolated for an extended period of time before entering the
Americas and that the founder haplotypes arose in situ in Beringia.
Once in the Americas, these immigrants spread southward.
Therefore, the phylogeographic distribution of this diversity can
provide insights into the mode of the initial phase of the peopling
of the Americas. A nested hierarchy of diversity from north to
south in Native American founding haplogroups would reflect
a gradual peopling, whereas a uniform distribution of Native
American founding haplotypes both in North and South America
implies a rapid occupation.
Previous studies of mtDNA variation recognized no major
subclade structure within each New World haplogroup ,[3–
4],. A few studies of mtDNA variation suggested subclade
structure ,,, but lacked the power to convincingly
demonstrate it. In this study we identified three sub-clades - C1b,
C1c and C1d - that incorporate nearly all of Native American
haplogroup C mtDNAs. All three are widely distributed in the
New World. They are absent in Asia, and show similar
coalescence times of approximately 13,90062,700 years ago
(Figure 1). Similar coalescence times were estimated for the other
major founder haplogroups - A2, B2 and D1 - suggesting the
simultaneous divergence of all founder clades across North and
South America. A different C1 sub-clade in Asia - C1a - likely
derives from the same ancestral population as the three Native
American sub-clades. Thus C1b, C1c and C1d are likely
independent New World founders. In addition to C1 sub-clades,
we defined two additional founders–D4h3 and C4c. These differ
by several mutations from the Asian-derived ancestral clades, D4h
and C4, respectively (Figure S1d,c). Haplogroup D4h3 ranges
from Alaska to Tierra del Fuego and has recently been identified
in Alaskan skeletal remains (10,300 ybp) . We identified
haplogroup C4c in two Ijka-speakers from Colombia, but its
distribution in the Americas remains poorly characterized.
Our phylogeographic analysis of a new mitochondrial genome
dataset allows us to draw several conclusions. First, before
spreading across the Americas, the ancestral population paused
in Beringia long enough for specific mutations to accumulate that
separate the New World founder lineages from their Asian sister-
clades (Figure 2) ,, [28–29]. Second, founding haplotypes
are uniformly distributed across North and South America instead
of exhibiting a nested structure from north to south (Figure 1).
Thus, after the Beringian standstill, the initial North to South
migration was likely a swift pioneering process, not a gradual
diffusion. This scenario matches the pattern of distribution of the
first archaeological sites in Northeast Asia and the Americas
,. Third, the largely autochthonous pattern of variation
Table 1. Defining mutations for Native American mtDNA haplogroups
HgHVS I HVS IICoding region
A16223-16290-1631973-235-263 663, 1736, 4248, 4824, 8794
A216111-16223-16290-16319-16362 64-73-146-153-235-2638027, 12007
A2a 16111-16223-16290-16319-16362 64-73-146-153-235-2633330
B4bd16189-1621773-263 827, 15535
B4b16189-1621773-263 499, 4820, 13590
B216189-16217 73-263 3547, 4977, 6473, 9950, 11177
C16223-16298-1632773-249d-263 3552A, 9545, 11914, 13263, 14318
C1b16223-16298-16325-16327 73-249d-263-290-291d 493
C416223-16298-1632773-249d-2632232iA, 6026, 11969, 15204
C4c16223-16245-16298-1632773-26311440, 13368, 14433, 15148
D416223-1636273-2633010, 8414, 14668
D216129-16223-16271-1636273-2633316, 7493, 8703, 9536, 11215
D4h316223-16241-16301-16342-1636273-2633336, 3396, 3644, 5048, 6285, 8949, 9458, 13135
D316223-16319-1636273-263951, 8020, 10181, 15440, 15951
X16189-16223-1627873-153-2636221, 6371, 13966, 14470
X2a16189-16213-16223-1627873-153-195-200-2631719, 8913, 12397, 14502
The full substitutional motif is shown in control region, the sub-clades defining mutations are indicated in bold.
Native American mtDNAs
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Figure 1. Schematic representation of phylogeny of human mtDNA outside of Africa. Branches encompassing Native Americans and their
immediate Asian ancestral and sister lineages, represented by complete sequences, are shown in black with coalescence ages indicated and
geographic location identified by colours. Lineages in brown correspond to the main haplogroups, found in Eurasia and Oceania, but absent in
Native Americans. For complete phylogenetic tree see Supplementary figure 1.
Native American mtDNAs
PLoS ONE | www.plosone.org3September 2007 | Issue 9 | e829
seen in Native American mtDNAs suggests that the swift migration
was followed by long-term isolation of local populations accom-
panied with the development of regional haplotypes within
continental founder haplogroups .
In addition to illuminating the peopling process during the
pioneering phase, the new dataset allows identification of more-
recent genetic exchanges around and across Beringia (Figure 2).
Specifically, haplogroup D2 consists of two sister clades, one found
only in Siberia (D2b) and the other found in northernmost
Eskimos, Chukchi, Aleut, and Athapaskans (D2a). While sub-
haplogroup D2a is shared between ethno-historically close related
Beringian Aleuts and Eskimos, (Figure S1) its sister clade D2b is
spread among populations from distantly related linguistic groups
(Tungusic, Turkic, Mongolic) (Table S2). A close relationship of
matrilineal ancestry between individuals from different linguistic
groups may be due to an overlap of geographic range of their
ancestors approximately at the time of the Pleistocene-Holocene
boundary. Alternatively, some populations may have received the
D2b variant through more recent gene flow. It is also worthwhile
to note the absence of D2 in all other Native American
populations, suggesting that D2 diversified in Beringia after the
initial migration into the Americas had occurred. Haplogroup D3
may have also reached America through more recent genetic
exchange. It is spread in Nganasans, Mansi, Evenks, Ulchi, Tuvas,
Chukchi and Siberian Eskimos , and recently reported in
Greenland and Canadian Inuit populations , but absent in
other Native Americans. Additional investigatios of these popula-
tions may provide insight into the cause of the phylogenetic
Surprisingly, we also found a Native American sub-type of
haplogroup A2 among Evenks and Selkups in southern and
western Siberia (Table S2). Previously, this HVS I motif is
reported in one Yakut-speaking Evenk in northwestern Siberia
. A novel demographic scenario of relatively recent gene flow
from Beringia to deep into western Siberia (Samoyedic-speaking
Selkups) is the most likely explanation for the phylogeography of
haplogroup A2a, which is nested within an otherwise exclusively
Native American A2 phylogeny (Figure S1).
The high-resolution sequence data analyzed in this study reveals
previously hidden diversity within the Native American mtDNA
gene pool. The new data suggest that the initial founders of the
Americas emerged from a single source ancestral population that
evolved in isolation, likely in Beringia. This scenario is consistent
with the unique pattern of diversity from autosomal locus
D9S1120  of a private allele in high frequency and ubiquitous
in the Americas. The finding that humans were present at the
Yana Rhinoceros Horn Site dated to 30,000 ybp  suggests that
the isolation in Beringia might have lasted up to 15,000 years.
Following this isolation, the initial founders of the Americas began
rapidly populating the New World from North to South America.
MATERIALS AND METHODS
The sample-set comprises 601 Native American individuals from
20 populations distributed throughout the Americas (23 Dogribs
from Subarctic Canada; 20 Apaches, 20 Northern Paiutes, 11
Zunis from Southwest US; 77 Ngo ¨bes, 34 Kunas from Panama; 39
Emberas, 57 Waunanas from Panama and Colombia; 47 Arsarios,
48 Koguis, 29 Ijkas, 42 Wayuus, 27 Coreguajes, 22 Vaupes from
Colombia; 12 Secoyas-Sionas, 32 Cayapas from Ecuador; 9
Tucuman, 18 Salta, 25 Catamarca, 5 Mocovi from Argentina) and
3764 samples from 26 Asian populations (51 Eskimos; 155
Chukchi; 120 Selkups; 66 Kets; 70 Tundra Nenets; 275 Tuvas;
185 Khakas; 339 Altaians; 170 Shors; 71 Koryaks; 85 Nanais; 122
Uyghurs; 406 Kazakhs; 58 Gilyaks; 61 Oroks; 105 Kirghiz; 48
Uzbeks; 38 Tajiks; 201 Buriats; 324 Evenks; 105 Evens; 22
Yukaghirs; 423 Yakuts; 157 Dolgans; 107 Nganasans). A subset of
these sequences were reported elsewhere [34–42].
First, haplogroup affiliations of the individual samples were
determined through RFLP analysis and DNA sequencing of the
HVS I region, if not known earlier [34–42]. Samples that could
not be assigned to haplogroups A–D or X were investigated for
evidence of recent admixture, particularly among populations with
well established historical accounts of co-existence of Native
American and either European or African populations. Samples of
European or African origin were excluded from the current study.
Further, 20 Native American and 7 Asian samples were selected
for complete sequencing of mtDNA genomes. Using these 27
novel and 113 published Native American and relevant Asian
complete or coding region sequences ,,,[43–50],
phylogenetic trees were reconstructed based on a maximum
parsimony approach (Figure S1, Text S1). From these whole
mtDNA genomes coding region markers were selected for
screening in the sample set through RFLP analyses or direct
sequencing (Table S1). Hierarchical method was used, so, that
each Native American sample was first cheked for nucleotide
positions, where a polymorphism could be assumed based on the
HVS I information and close ethnic, geographic or linquistic
affiliation to complete sequenced sample. From Asian populations,
Figure 2. Schematic illustration of maternal geneflow in and out of
Beringia. Colours of the arrows correspond to approximate timing of
the events and are decoded in the coloured time-bar. The initial
peopling of Berinigia (depicted in light yellow) was followed by
a standstill after which the ancestors of the Native Americans spread
swiftly all over the New World while some of the Beringian maternal
lineages–C1a-spred westwards. More recent (shown in green) genetic
exchange is manifested by back-migration of A2a into Siberia and the
spread of D2a into north-eastern America that post-dated the initial
peopling of the New World.
Native American mtDNAs
PLoS ONE | www.plosone.org4September 2007 | Issue 9 | e829
samples, which could be relevant to Native American hap-
logroups, were selected based on HVS I sequence and analyzed for
coding region markers (A2–12007, 8027; A2a–3330; C1a–3826,
7598; C4–11969; C4a–12672; C4b–3816; C4c–11440; D2–8703;
D2a–4991, 11959; D2b–9181; D4–8414T; D4a–3206; D4e1–
3316; D4h–3336, 3644; D4m–9667; D5–5301; D5a–11944,
DNA was extracted using conventional methods [34–42].
Preparation of sequencing templates was carried out following
standard protocols, employing FIREPol polymerase (Solis Bio-
Dyne). Purified products were sequenced with the DYEnamicTM
ET terminator cycle sequencing kit (Amersham Pharmacia
Biotech) and analyzed on MegaBace1000 or ABI 3730xl
sequencers. Sequences were aligned and analyzed with the
Wisconsin Package (GCG) or ChromasPro 1.34.
Coalescence-age calculations and SDs were estimated based on
the phylogenies of complete sequences ,. Given the global
propensity of young mtDNA clades showing a significant excess of
non-synonymous mutations, application of the raw molecular
clock  in intra-species data sets is problematic . Therefore,
for dating the coalescent times of founder haplogroups we
employed only synonymous transitions between the np 577-
16023, assuming the rate of 3.5610-8 (SD 0.1610-8)/year/
position . The complete mtDNA genome data can be found in
Found at: doi:10.1371/journal.pone.0000829.s001 (0.10 MB
Complete Phylogenetic Trees
Found at: doi:10.1371/journal.pone.0000829.s002 (0.03 MB
Legend for Figure S1.
Found at: doi:10.1371/journal.pone.0000829.s003 (0.71 MB
Found at: doi:10.1371/journal.pone.0000829.s004 (0.02 MB
We would like to thank the late John McDonough and the late Dr.
Surinder Papiha for their contributions to this research project.
Conceived and designed the experiments: TK RM. Performed the
experiments: ET MR. Analyzed the data: CB MM TK RM ET MR.
Contributed reagents/materials/analysis tools: CB CM RV TK RM DS
OR CM EK SF MG VS MG SZ LO LD MV JD. Wrote the paper: CM
RV MM TK RM ET DS.
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PLoS ONE | www.plosone.org6September 2007 | Issue 9 | e829