american indian prehistory as written in the mitochondrial dna: a review

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American Indian Prehistory as Written in the Mitochondrial DNA:A ReviewAuthor(s) :Douglas C. Wallace and Antonio TorroniSource: Human Biology, 81(5/6):509-521. 2009.Published By: Wayne State University PressDOI: http://dx.doi.org/10.3378/027.081.0602URL: http://www.bioone.org/doi/full/10.3378/027.081.0602

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Human Biology, June 1992, v. 64, no. 3, pp. 403–416.

Copyright © 1992 Wayne State University Press, Detroit, Michigan 48202

American Indian Prehistory as Written in the Mitochondrial DNA: A Review

douglas c. wallace1 and antonio torroni1

Abstract Native Americans have been divided into three linguistic groups:

the reasonably well- defined Eskaleut and Nadene of northern North America

and the highly heterogeneous Amerind of North, Central, and South Amer-

ica. The heterogeneity of the Amerinds has been proposed to be the result

of either multiple independent migrations or a single ancient migration with

extensive in situ radiation. To investigate the origin and interrelationship of

the American Indians, we examined the mitochondrial DNA (mtDNA) varia-

tion in 87 Amerinds (Pima, Maya, and Ticuna of North, Central, and South

America, respectively), 80 Nadene (Dogrib and Tlingit of northwest North

America and Navajo of the southwest North America), and 153 Asians from 7

diverse populations. American Indian mtDNAs were found to be directly de-

scended from five founding Asian mtDNAs and to cluster into four lineages,

each characterized by a different rare Asian mtDNA marker. Lineage A is

defined by a HaeIII site gain at np 663, lineage B by a 9- bp deletion between

the COII and tRNALys genes, lineage C by a HincII site loss at np 13259,

and lineage D by an AluI site loss at np 5176. The North, Central, and South

America Amerinds were found to harbor all four lineages, demonstrating that

the Amerinds originated from a common ancestral genetic stock. The genetic

variation of three of the four Amerind lineages (A, C, and D) was similar with

a mean value of 0.084%, whereas the sequence variation in the fourth lineage

(B) was much lower, raising the possibility of an independent arrival. By

contrast, the Nadene mtDNAs were predominantly from lineage A, with 27%

of them having a Nadene- specific RsaI site loss at np 16329. The accumu-

lated Nadene variation was only 0.021%. These results demonstrate that the

Amerind mtDNAs arose from one or maybe two Asian migrations that were

distinct from the migration of the Nadene and that the Amerind populations

are about four times older than the Nadene.

Questions about Native American Prehistory

When Columbus contacted the Americas in 1492, Native American occupa-

tion stretched from the Bering Strait to Tierra del Fuego. These native populations

encompassed extraordinary linguistic and cultural diversity, which has fueled ex-

tensive debate on their interrelationships and origins.

1 Center for Genetics and Molecular Medicine, Emory University, Atlanta, GA 30322.

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510 / wallace and torroni

Traditional anthropological analysis has confirmed that American Indians

came from Asia, probably crossing the Bering land bridge when it was exposed

during an episode of glaciation (Crawford and Enciso 1983; Fladmark 1983;

Laughlin and Wolf 1979; Matson et al. 1968; Schell and Blumberg 1988; Turner

1983, 1987; Williams et al. 1985). Linguistic and genetic analysis has divided

the Native Americans into three major groups: Eskaleut, Nadene, and Amerind

(Cavalli- Sforza et al. 1988; Greenberg 1987; Neel 1978; Neel and Thompson

1978; Szathmary 1984, 1991). The first two groups are well defined, with the

Eskaleut encompassing the Eskimos and the Aleuts of the Arctic and the Nadene

including the Athapaskans, Tlingits, Haida, and Eyaks of northwestern North

America. The homogeneity of these linguistic groups has led to the hypothesis

that they represent two separate waves of migration that arrived about 5000 and

9000 years or more before present. By contrast, the Amerind group, composed of

the American Indians from North, Central, and South America, shows extensive

linguistic diversity. This diversity has been proposed to be the result of the amal-

gamation of multiple independent migrations with different linguistic traditions

or of a single ancient migration that has undergone extensive linguistic radiation

(Greenberg et al. 1986).

Archeological evidence on the timing of ancestral American Indian migra-

tions is also ambiguous. The oldest skeletal remains and Clovis lithic artifacts have

yielded dates between 13,000 and 14,000 years b.p. (Nelson et al. 1986; Taylor et

al. 1985). By contrast, excavations at the Meadowcroft Rock Shelter in Pennsyl-

vania (Adovasio et al. 1983), the Boqueiro site in Pedra Furada in Brazil (Guidon

and Delibrias 1986), and the Monte Verde site in Chile (Dillehay and Collins 1988)

have yielded evidence of human occupation dating back to 33,000 years b.p., al-

though the authenticity of these sites continues to be debated (Marshall1990).

These observations generate a number of questions. How many Asian mi-

grations occurred? When did the ancestral American Indians arrive? And what

is the relationship between the Amerinds and the Nadene? Recently, molecular

anthropology has begun to provide new insights into these questions. One particu-

larly productive approach has been the analysis of mitochondrial DNA (mtDNA)

variation.

mtDNA Variation and Human Origins

mtDNA has several unique features that make it ideal for studying ancient

human migrations. mtDNA is a small circular molecule of 16,569 nucleotide pairs

(np). It is present in 3000–5000 copies per cell (Shuster et al. 1988), making it easy

to analyze. mtDNA is maternally inherited (Case and Wallace 1981; Giles et al.

1980) and never recombines (Schurr et al. 1990). Therefore it evolves by the se-

quential accumulation of mutations along radiating female lineages (Johnson et al.

1983). Finally, its sequence evolves about 10 times faster than nuclear DNA (Brown

et al. 1979, 1982; Miyata et al. 1982; Neckelmann et al. 1987; Wallace et al. 1987),

permitting distinctions to be made between even closely related populations.

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American Indian Prehistory and mtDNA / 511

The mtDNA codes for 13 polypeptides of mitochondrial respiratory com-

plexes and for the rRNA and tRNA genes for mitochondrial protein synthesis

(Shoffner and Wallace 1990). These coding regions evolve at a rate of 2–4% per

million years (Cann et al. 1987; Stoneking et al. 1990) with the replacement muta-

tion rate being 1.8 × 10–9 substitutions per site per year (SSY) (0.19% per million

years), whereas the synonymous mutation rate is 32.3 × 10–9 SSY (3.2% per mil-

lion years) (Wallace et al. 1987). The noncoding D- loop sequence evolves much

faster, 8.4% per million years (Greenberg et al. 1983; Horai and Hayasaka 1990;

Vigilant et al. 1989). Thus analysis of various regions of the mtDNA can provide

information on different time scales (Di Rienzo and Wilson 1991; Stoneking et al.

1991; Vigilant et al. 1991).

Sequence variation of the mtDNA can be efficiently surveyed through re-

striction fragment length polymorphisms (RFLPs). Restriction fragment vari-

ants are detected by gel electrophoresis, and each restriction site gain or loss is

equivalent to a single nucleotide substitution. One efficient procedure for analyz-

ing RFLPs is to digest blood cell DNAs, resolve the fragments on agarose gels,

and detect the fragments by Southern blotting and hybridization with radioac-

tive mtDNA probes (Blanc et al. 1983; Denaro et al. 1981; Johnson et al. 1983;

Wallace 1983). Six highly informative (core) restriction endonucleases (HpaI,

BamHI, HaeII, MspI, AvaII, and HincII) have been used to survey the variation

of 3065 individuals from 62 geographic samples. This survey has detected 149

haplotypes encompassing 81 polymorphic sites (Blanc et al. 1983; Bonné- Tamir

et al. 1986; Brega, Gardella et al. 1986; Brega, Scozzari et al. 1986; Denaro et al.

1981; Johnson et al. 1983; Merriwether et al. 1991; Santachiara- Benerecetti et al.

1988; Semino et al. 1989, 1991; Scozzari et al. 1988; Torroni et al. 1990).

These studies have revealed four principles of human mtDNA evolu-

tion. First, mtDNA mutations accumulate sequentially along radiating maternal

lineages. Second, mtDNA variation correlates highly with the ethnic and geo-

graphic origin of the samples, because new mutations occurred concurrently with

the migration of female lineages into new geographic regions. Third, all human

mtDNAs are components of a single mtDNA lineage, indicating a single origin.

Fourth, the mtDNA tree and hence our species are very young. The average age

of the ethnic groups is about 100,000 years b.p., and the overall lineal age is about

twice that, with the greatest mtDNA diversity found in Africa. If we assume that

the evolutionary rate of the mtDNA is constant, then the origin of the mtDNA tree

and hence of Homo sapiens must be Africa. These principles were first reported

by Johnson et al. (1983) and have subsequently been confirmed (Cann et al. 1987;

Merriwether et al. 1991; Vigilant et al. 1991).

mtDNA Variation in American Indians

The high correlation between mtDNA variation and ethnic and geographic

origin suggested that mtDNA variation might be valuable for determining the

number and origin of ancient Asian migrations to the Americas. This has proven

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to be the case. It is now known that the Amerinds are a coherent genetic group

that originated from a common ancestral genetic stock and that the Nadene are a

separate group that arrived in the Americas much later.

The first evidence that the Amerinds represent a genetically homogeneous

population came from analyzing the mtDNAs of the Pima and Papago of the

southwestern United States. RFLP analysis using the six core restriction endo-

nucleases revealed that the mtDNAs of the Pima and Papago were much less

variable than those of Asians but harbored certain rare Asian variants at high

frequencies. An individual restriction pattern generated by one restriction endo-

nuclease is called a morph, and analysis with HpaI, BamHI, HpaII, and AvaII

revealed that the Pima and Papago harbored only the most common Asian morph.

Analysis with HaeII revealed somewhat greater variation, with about 8% of the

Pima and Papago mtDNAs having variants found at low frequencies in Asians and

Europeans. However, analysis with HincII revealed that an extraordinary 41% of

the Pima and Papago harbor the rare Asian variant HincII morph 6 and that an ad-

ditional 3% had an American Indian–specific derivative, HincII morph 9 (Wallace

et al. 1985). HincII morph 2 is the most common morph in Asians (Blanc et al.

1983) and was found in 55% of the Pima and Papago. The loss of restriction site

e at np 13259 converts HincII morph 2 to morph 6, a mutation that presumably

occurred in Asia. The subsequent loss of the adjacent site c at np 13634 results

in HincII morph 9 and occurred in the Americas (Wallace et al. 1985) (Figure 1).

Because HincII morph 6 has been found in only 2% of Asian mtDNAs and not in

European or African mtDNAs (Blanc et al. 1983), these results confirm the Asian

origin of the Amerinds. In addition, the over 20- fold increase in the frequency of

HincII morph 6 mtDNAs indicates that a major bottleneck occurred during the

transition from the Asians to the southwestern Amerinds.

The genetic bottleneck was shown to have occurred before the radiation of

the ancestral Amerinds by analyzing Central American Maya and South Ameri-

can Ticuna mtDNAs. Like the Pima and Papago, the Maya and the Ticuna were

monomorphic for HpaI and BamHI and showed only modest variation for MspI/

HpaII, HaeII, and AvaII. However, HincII was again polymorphic with 11% of the

Mayan mtDNAs and 42% of the Ticuna mtDNAs being HincII morph 6. Hence all

the Amerinds harbored the same rare Asian marker at a high frequency, confirm-

ing that they descended from a common stock (Schurr et al. 1990).

The genetic association of all Amerinds was further substantiated by analy-

sis of an Asian- specific 9- bp intergenic deletion between the COII and tRNALys

genes (Cann and Wilson 1983; Wrischnik et al. 1987). This variant identifies an

mtDNA lineage that is different from that associated with HincII morph 6. Analy-

sis of Amerind mtDNAs revealed that 45% of the Pima mtDNAs and 22% of

the Maya mtDNAs contain this morph (Schurr et al. 1990; Torroni et al. 1992).

Although the Ticuna do not harbor this mtDNA, many other Central and South

American tribes do (unpublished data). Hence the COII/tRNALys deletion defines

a second Asian mtDNA lineage shared with Amerinds and confirms the common

origin of these populations (Schurr et al. 1990).

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To clarify the relationship between Asian and American Indian mtDNAs,

we analyzed 153 Asian mtDNAs and 167 American Indian mtDNAs using poly-

merase chain reaction (PCR) amplification of the mtDNA in 9 overlapping seg-

ments and digestion of each segment with 14 restriction endonucleases (AluI,

AvaII, DdeI, HaeIII, HhaI, Hinfl, HpaI, HpaII, MboI, RsaI, TaqI, BamHI, HaeII,

and HincII). The Asian samples included 14 Malaysian Chinese, 32 Malaysian

Senoi, 14 Malays, 32 Borneans, 28 Vietnamese, 20 Han Chinese from Taiwan,

and 13 Koreans (Ballinger et al. 1992). The Americans Indians included 87 Am-

erinds (30 Pima, 27 Maya, 28 Ticuna, 1 Pomo, and 1 Hopi) and 80 Nadene (2

Tlingit, 30 Dogrib, and 48 Navajo) (Torroni et al. 1992).

The Asians were found to harbor extensive mtDNA variation, including

106 haplotypes encompassing 191 polymorphic restriction site (Ballinger et al.

1992). The COII/tRNALys deletion was found to have occurred more than once.

However, most of the mtDNAs associated with the deletion were derived from a

single ancient event and have closely related haplotypes. The highest Asian fre-

quency (40%) of this deletion lineage is in the Han Chinese of Taiwan. This sug-

gests that this mtDNA lineage arose in southeast China (Ballinger et al. 1992). Its

frequency then declines along the southern Asian coast and increases again into

Figure 1. Restriction endonuclease fragment patterns of HincII morphs 2, 6, and 9. Uppercase let-

ters correspond to fragments found in the circular map of the most common morph, HincII

morph 2. Lowercase letters indicate positions of site losses converting morph 2 to morph 6

(e + d) and morph 6 to morph 9 (f). Reprinted from Wallace et al. (1985) with permission.

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the Pacific, where it approaches fixation, being present in 93% of Polynesians

(Ballinger et al. 1992; Hertzberg et al. 1989; Stoneking et al. 1990). American

Indian deletion mtDNAs are also derived from this lineage, the deletion accom-

panying migrants who colonized both the Americas and the Pacific. The Viet-

namese have the greatest intragroup mtDNA variation (0.236%), indicating that

they are the oldest population. They also have the highest frequency of mtDNAs

that are HpaI/HincII morph 1 (Ballinger et al. 1992), an mtDNA morph previ-

ously proposed to identify a founding Asian mtDNA lineage (Blanc et al. 1983).

Hence most Asian mtDNA variation centers around southeastern China, suggest-

ing that this is where the Asian population originated. Two additional ancient

mtDNA restriction site polymorphisms were found to divide all Asian haplotypes

into two groups: a DdeI site at np 10394 and an overlapping AluI site at np 10397

(Ballinger et al. 1992).

Compared with the Asian mtDNAs, American Indian mtDNAs show sub-

stantially less variation, with 50 haplotypes (Table 1) encompassing 68 poly-

morphic sites (Torroni et al. 1992). All the American Indian mtDNA haplotypes

separated into four discrete lineages (A, B, C, and D) (Figure 2), and each lineage

was founded by mtDNA haplotypes (1, 9, 13, 43, and 44) that were either closely

related to or identical with haplotypes found in Asia (Ballinger et al. 1992; Tor-

roni et al. 1992). Lineages A and B differ from lineages C and D in that the former

lack the Asian DdeI np 10394 and AluI np 10397 sites. Furthermore, each lineage

is defined by a specific Asian polymorphism: lineage A by an HaeIII site gain at

Table 1. Mitochondrial DNA Haplotype Distribution in Nadene and Amerindsa

mtDNA

Lineage A Lineage

1 1 1 1 1 1 1 1 1 1 2 Population N 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0

Nadene

Dogrib 30 19 7 1 3

Tlingit 2 1 1

Navajo 48 11 13 4 11 2 1 2 1 1

Amerinds

Hopi 1

Pima 30 2 5 1 1

Pomo 1

Maya 27 5 2 2 2 1 1 1 5

Ticuna 28 2 1 2

Total 167 36 2 2 2 21 1 2 1 11 1 1 1 21 2 1 2 1 1 1 1

Modified from Torroni et al. (1992).

a. We define a lineage as a set of mtDNAs related to each other by shared common and unique mu-

tations not observed in other mtDNAs. We define a haplotype as a distinct association of restriction

endonuclease site polymorphisms for 14 enzymes within 1 mtDNA genome.

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np 663, lineage B by the 9- bp deletion, lineage C by the HincII site loss at np

13259 (HincII morph 6), and lineage D by an AluI site loss at np 5176. Beyond

the founding haplotypes (9, 13, 43, and 44), all the mtDNAs of these lineages

are American Indian specific, indicating that they arose after the separation of

these lineages from Asians. The Amerinds (Figure 2, filled circles) encompass all

four lineages, and the Amerind intracluster mtDNA variation of three of these is

similar (0.071% for lineage A, 0.102% for lineage C, and 0.073% for lineage D).

This suggests that their founding haplotypes became isolated at approximately

the same time. The weighted- average intracluster variation of these lineages is

0.084%. Assuming an mtDNA evolutionary rate of 2–4% per million years, these

lineages would be between 21,000 and 42,000 years old (Torroni et al. 1992).

The Nadene mtDNAs (Figure 2, open circles) were much less variable than

those of the Amerinds. The Tlingit and Dogrib mtDNAs of Alaska and Canada

all fall into cluster A, defined by the HaeIII np 663 site gain, and only four hap-

lotypes (Torroni et al. 1992) were observed (Table 1). Furthermore, haplotypes

5 and 6 carried a distinctive RsaI site loss at np 16329, which provides a unique

marker for Nadene mtDNAs. The Navajo mtDNA also contained haplotypes 1, 5,

and 9, confirming their affinity with the northwestern Nadene. However, the Na-

vajo mtDNA also contained six deletion haplotypes (Table 1, Figure 2). Because

the ancestors of the Navajo and the Apache migrated through the Great Plains to

the southwestern United States about 1000 years ago, a reasonable hypothesis

is that these deletion mtDNAs were acquired by the Navajo through admixture

with Amerinds of the southwestern United States (Torroni et al. 1992). Consis-

tent with the limited number of haplotypes, the Nadene mtDNA diversity was

only 0.021%, about one- fourth that of the Amerinds. This means that the Nadene

Haplotype

B Lineage C Lineage D

2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 4 4 5 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0

2

1

1 2 1 1 3 1 1 1 5 3 1 1

1

1 1 1 1 2 1 1

1 3 2 3 4 1 4 2 3

1 1 2 1 1 3 1 1 2 1 1 1 1 1 5 1 3 1 1 3 2 3 2 5 1 4 2 3 1 1

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mtDNA lineage is 5250–10,500 years old (Torroni et al. 1992), a time range con-

sistent with estimates from linguistic diversity (Greenberg 1987).

The relationship of lineage B to the Amerinds is less clear. Its sequence

divergence is 0.038%, a value greater than that of Nadene lineage A and lower

than those calculated for the rest of the Amerind lineages. This result raises the

possibility that the individuals carrying the founding haplotype of lineage B ar-

rived in the Americas in a separate migration that occurred after the first migration

and before the migration of the ancestral Nadene. As these migrants moved south,

they would have mixed with the descendants of the original settlers.

These studies lead to the conclusion that all modern Amerinds essentially

derived from a common ancestral genetic stock. Four of the founding mtDNA

haplotypes (1, 9, 43, and 44) arrived with the first human migrants in the Ameri-

cas. Possibly, haplotype 13, the founding haplotype of the 9- bp deletion lineage,

arrived independently and more recently. These results confirm the hypothesis that

the diversity of the Amerind linguistic group was essentially generated through ra-

diation from a single founding language (Greenberg 1987; Greenberg et al. 1986).

They also show that the Nadene were derived from a different founding popula-

tion that developed much more recently than the Amerinds. The overall age of

three of the four Amerind mtDNA lineages is 21,000 to 42,000 years, an estimate

that is consistent with the ages of the oldest archeological sites. However, it is

currently unclear whether the founder effect that isolated these mtDNA lineages

occurred as Asians migrated across the Bering land bridge or as they migrated into

the Siberian steppes. Hence, to complete the story of American Indian origins, we

must analyze the mtDNA variation of Siberians, their closest related Asian popu-

lation (Posukh et al. 1990).

Received 3 July 1991; revision received 8 November 1991.

Figure 2. Phylogenetic tree of Native American mtDNA haplotypes. A, B, C, and D indicate the

four haplotype lineages, with the key below the dendrogram indicating the characteristic

mutation of each one. The numbers at the end of each branch refer to distinct mtDNA

haplotypes (Tables 1 and 2), with solid circles indicating those present in Amerinds, open

circles indicating those present in Nadene, and shaded circles indicating those present in

both groups. hypanc is the hypothetical ancestor [from Cann et al. (1987)]. Individual

branch lengths are proportional to the number of mutational steps between haplotypes.

Haplotypes 28 and 29 lack characteristic Native American mutations and do not cluster in

any of the four lineages. Because they have mutations observed in whites, they were prob-

ably introduced by European admixture. This dendogram was inferred using parsimony

analysis (PAUP, version 3.0m; Swofford 1989), is 77 mutational steps in length with a

consistency index of 0.844, and is the consensus of 100 trees generated by the tree bisec-

tion and reconnection (TBR) method. Intragroup sequence divergences of each lineage

were calculated according to the method of Nei and Tajima (1983). Modified from Torroni

et al. (1992).

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