Mitochondrial DNA Studies of Native Americans: Conceptions and Misconceptions of the Population Prehistory of the Americas JASON A

Home , Haplogroup A (mtDNA), Haplogroup A (Y-DNA), Haplogroup B (mtDNA), Haplogroup C (mtDNA), Haplogroup H (mtDNA), Haplogroup V (mtDNA)

Evolutionary Anthropology 7

ARTICLES

Mitochondrial DNA Studies of Native Americans: Conceptions and Misconceptions of the Population Prehistory of the Americas JASON A. ESHLEMAN, RIPAN S. MALHI, AND DAVID GLENN SMITH

A decade ago, the first reviews of the collective mitochondrial DNA (mtDNA) data from gional patterning among native popu- Native Americans concluded that the Americas were peopled through multiple migrations lations of North America. All four from different Asian populations beginning more than 30,000 years ago.1 These reports haplogroups are shared with Asian confirmed multiple-wave hypotheses suggested earlier by other sources and rejected the populations, confirming the conclu- dominant Clovis-first archeological paradigm. Consequently, it appeared that molecular sions of classical genetic studies that biology had made a significant contribution to the study of American prehistory. As Cann2 the first Americans migrated from comments, the Americas held the greatest promise for genetics to help solve some of the Asia across the Bering land bridge.4,5 mysteries of prehistoric populations. In particular, mtDNA appeared to offer real potential as Early analyses of restriction fragment a means of better understanding ancient population movements. A decade later, none of the length polymorphism in the entire mi- early conclusions remain unequivocal. Nevertheless, in its maturity, the study of Native tochondria genome showed that these American mtDNA has produced a volume of reports that still illuminate the nature and timing four major clades could be readily dis- of the first peopling and postcolonization population movements within the New World. tinguished by the gain or loss of one or more restriction sites or by the For several reasons, mtDNA has for studying prehistory. The human presence or absence of a 9 base-pair been regarded as particularly useful mitochondrion is an extra nuclear or- deletion in the COII-tRNAlys inter- ganelle having DNA that exists as a genic regions.5 Torroni and cowork- circular molecule 16,569 base pairs in ers7 found that diagnostic mutations length, in which all nucleotide posi- in the CR accompanied the restriction Jason A. Eshleman is a postdoctoral re- tions and coding loci are known.3 Be- markers and the fragment deletion searcher at the University of California, cause this DNA is uniquely maternally that characterize the four haplo- Davis, where he completed his doctoral research examining mtDNA extracted inherited and, unlike nuclear DNA, groups, as is expected of a nonrecom- from prehistoric California sites. He has does not recombine, all changes in bining DNA molecule. Each haplo- coauthored a number of publications ex- mtDNA sequence are the result of ac- amining mtDNA diversity in the New group could be further divided into World. E-mail: [email protected]. cumulated mutations inherited from subclades or discrete haplotypes Ripan S. Malhi is a postdoctoral researcher mother to daughter. In addition, based on additional restriction frag- in the Department of Human Genetics at University of Michigan in Ann Arbor. He has mtDNA mutates an order of magni- ment length polymorphisms or spe- conducted his doctoral research on Native tude faster than does nuclear DNA, cific CR mutations. American migrations in the northeastern with the control region mutating at an and southwestern United States with mod- Although corresponding haplo- ern mtDNA, as well as an analysis of an- even greater rate, making it particu- groups can be found in various Asian cient DNA from the Columbia Plateau. He larly useful for analyses at shallow populations, only founding haplo- has recently authored (with Drs. Eshleman time depths. Finally, mtDNA exists in and Smith) an analysis of mtDNA diversity types of the New World are shared across North America. high copy number in haploid condi- between the two continents, again David Glenn Smith is a professor of anthro- tion. Consequently, it is easily assayed pology at the University of California, Davis. confirming that the Americas were He directs research in Native American ge- in the laboratory and can be recovered initially settled by a limited number of netic variation ancient mtDNA analysis as from prehistoric biological material female immigrants from Asia whose well as non-human primate genetics. Un- in sufficient quantities for amplifica- der his direction, the laboratory of molecu- mtDNA underwent subsequent evolu- lar anthropology at UC-Davis has been in- tion and analysis using the polymer- tion independent of its ancestral form vestigating human migrations with ancient ase chain reaction. 4 DNA from the Great Basin, the Columbia in Asia. The fact that shared haplo- Plateau, the Ohio River Valley, lower Great types on both sides of the Pacific are Lakes, Central California and Central Mex- uncommon has generated consider- ico. HAPLOGROUPS AND able debate as to the size and source HAPLOTYPES of the ancestral population (or popu- Key words: mtDNA, Native Americans, migra- Early studies of Native American lations), as well as the number of tions, ancient DNA mtDNA revealed four major clades, or waves of migration that came out of haplogroups, of haplotypes.4,5 Al- Asia. However, some haplogroups Evolutionary Anthropology 12:7–18 (2003) though they are broadly distributed share more than one haplotype with DOI 10.1002/evan.10048 6 Published online in Wiley InterScience throughout the Americas, these four Asia, and it is not clear whether the (www.interscience.wiley.com). haplogroups exhibit significant re- divergence they represent occurred in 8 Evolutionary Anthropology ARTICLES

Asia or the New World. This has made within-haplogroup diversity. Torroni high frequencies of haplogroup A but problematic the use of mtDNA diver- and colleagues7 noted that sequence lacked haplogroup B and exhibited sity to estimate the time of coloniza- diversity within haplogroups A, C, and only low frequencies of haplogroups C tion, the size and source of the ances- D was substantially greater than that and D, whereas Eskimo-Aleut popula- tral population, and the number of in haplogroup B for the populations tions appeared to have high frequen- waves of migration out of Asia. sampled. This, they argued, was evi- cies of haplogroups A and D but dence of a later migration of B matri- lacked haplogroups B and C. How- lines to the New World. The fact that ever, on closer inspection of a large WAVES OF MIGRATION haplogroups A, C, and D are found in number of samples, Merriwether, Although there has been little scien- Eastern Siberia, a likely staging point Rothhammer, and Ferrell16 demon- tific controversy about the Asian ori- for any trans-Beringian migration, strated that groups traditionally clas- gins of Native American populations, whereas haplogroup B is curiously ab- sified as Eskimo and Na-Dene had contention surrounds the question of sent from the region, is consistent measurable frequencies of all four the number of waves of migration. with this argument. These two early haplogroups when larger samples The Americas are home to approxi- migrations were argued to be inde- were assayed. Reasoning that it is un- mately half of the world’s language pendent of later migrations of Na- likely that separate migrations from stocks.8 This extraordinary linguistic Dene. However, this model did not ad- Asia would have introduced exactly diversity among the indigenous dress the relationship of Eskimos to the same four rare Asian types,20 Mer- groups of Native America suggests to other American populations. Because riwether, Rothhammer, and Ferrell16 many comparative linguists that there the Eskimos represent the most recent concluded that the Americas must was either a single colonization sev- arrivals in historical linguistic models have been peopled from a single eral tens of thousands of years ago or of the settlement of the New World, source. Postcolonization forces might that there were multiple colonizations the work of Torroni and coworkers7 subsequently have led to the regional by speakers of different unrelated lan- implies that there were as many as patterning in the Americas that ap- guage phyla.8 There is dispute, how- four independent migrations. peared to differentiate the three hy- ever, about whether or not linguistic Due to the pronounced regional pothesized linguistic phyla. Moreover, evidence supports an early8,9 or later patterning of mtDNA haplogroup and Lorenz and Smith17 showed that first occupation of the Americas.10 haplotype frequency distributions in when a larger, more regionally diverse The pattern of language diversity has the Americas, estimates of genetic di- sample of haplogroup B was analyzed, been used to support the tripartite diversity are strongly influenced by within-haplogroup diversity was not vision of Native American groups sampling. Moreover, little is known less than that for haplogroups A, C, widely popularized by Greenberg, about the actual number of initial col- and D. Further consideration that Turner, and Zegura.11 Although this onists or the population dynamics in- more than a single founding haplo- division initially was suggested much volved in colonizing a continent free type of one or more haplogroups sur- earlier,12 Greenberg, Turner, and Ze- of other humans. Indeed, the degree vives in modern Native American pop- gura11 proposed that the Amerind, to which Native American popula- ulations14,21 renders comparisons of Na-Dene, and Eskimo-Aleut exhibit tions experienced an initial founder diversity among the four haplogroups parallel genetic and morphometric effect or subsequent genetic bottle- moot vis-a`-vis their implications with differences that indicate three sepa- neck is itself controversial.14 respect to the number of independent rate migrations to the New World. Horai and coworkers15 hypothe- migrations to the Americas. Critics noted that the agreement sized that each haplogroup repre- The presence of all four haplo- among linguistics, morphology and sented an independent founding pop- groups in all three of Greenberg, genetics was not as consistent as ini- ulation. This view is not widely Turner, and Zegura’s11 language phyla tially had been claimed and, indeed, supported because a random selection could, of course, be the result of ad- the linguistic divisions themselves of even a small group of emigrants mixture after colonization. Neighbor- have not held up to persistent scruti- from Eastern Siberia today would ing Algonquian and Athabaskan pop- ny.13 Nonetheless, the model has have a high probability of including ulations both have the rare mutation strongly influenced designs for re- members of haplogroups A, C, and D. associated with Albumin Naskapi search on Native American popula- While earlier studies of Native Amer- (Al*Nas), possibly as a result of an- tion genetics. ican mtDNA seemed to support mul- cient admixture, given that the Atha- Early analyses of mtDNA indicated tiple waves, in line with linguistic baskan and Algonquian languages ex- that the distribution of haplogroups models of colonization, more recent hibit no evidence of a close or even and the levels of sequence divergence studies of mtDNA have supported remote linguistic relationship.22 How- among Greenberg, Turner, and Zegu- only a single movement out of ever, haplogroup frequencies alone ra’s linguistic phyla were the result of Asia.16–19 cannot distinguish between admix- multiple migrations. If the effective Single-wave arguments principally ture and common ancestry. Making founding population was small, only emerged from analyses of larger and this distinction requires a more exten- one matriline would be likely to have more diverse samples. The arguments sive analysis of the discrete haplo- survived each migration. Thus, mem- have followed two separate lines of types to determine if related types are bers of different haplogroups that en- evidence, though they are quite com- shared only between neighboring tered the New World at the same time patible. Early studies of Na-Dene pop- populations, suggesting admixture. should exhibit comparable levels of ulations suggested that they possessed Haplotype analyses are also consis- ARTICLES Evolutionary Anthropology 9 tent with the single-migration hypoth- mos, but only with a later reexpansion plete sampling or different methods of esis. The CR sequence of the great ma- out of the north. calculating diversity,25 these results jority of all Native American members While Bonatto and Salzano could are consistent with a single wave of of haplogroup A, regardless of linguis- not estimate the sequence divergence migration to the Americas. However, tic affiliation, shares a C3T transition of haplogroups B, C, and D in the Na- equal diversity within haplogroups at np16111 that is not seen in any Dene and Eskimo, in whom these hap- would be expected only if the number Asian populations except a few in logroups are rare, they did assess the of founding haplotypes is the same. Eastern Siberia, including the Chuk- relative diversity of haplogroups A, B, Indeed, future clarification of this dis- chi.19 The predominance of this C, and D in Amerinds. As in the anal- pute will require that we consider not marker in the Americas and its con- ysis of haplogroup distributions by only the level of diversity, but also the spicuous absence from Asia supports population structure, which might the view that this marker originated in give better clues to prehistoric ori- Beringia soon after its settlement. A gins.26–28 characteristic Native American form of haplogroup C that includes the That a particular marker WHERE DID THE FOUNDING C3T transition at np16325 and a is widespread in POPULATIONS ORIGINATE? form of haplogroup X that includes the T3C transition at np16213 are individuals classified as Based on geographic proximity both widespread in the Americas and Amerind, Eskimo, and alone, Eastern Siberia stands as a absent from Asia, suggesting a Bering- likely candidate for the source of the ian source for, and a single origin of, Na-Dene but does not Native American founder population. those haplogroups as well. That a par- occur in any Asian However, while haplogroups A, C, and ticular marker is widespread in indi- D are all found in Eastern Siberia, B is viduals classified as Amerind, Eskimo, source outside of conspicuously absent.29,30 While the and Na-Dene but does not occur in eastern Siberia suggests absence of haplogroup B from East- any Asian source outside of eastern ern Siberia might suggest an addi- Siberia suggests that speakers of all that speakers of all three tional migration, presumably from three of the proposed divisions have a of the proposed southern coastal Asia or South-Cen- common New World origin.19 More- tral China,31 where the 9 base pair over, Bonatto and Salzano19 reported divisions have a deletion is more common,29 it is also that the diversity of haplogroup A common New World possible that haplogroup B was among Greenberg, Turner, and Zegu- origin. Moreover, present in Eastern Siberia before the ra’s principle Native American lan- New World was colonized but has guage groupings was remarkably sim- Bonatto and Salzano since become extinct there.30 If this is ilar within each of the three linguistic reported that the not the case, Eastern Siberia is not a phyla. In addition to the C3T transi- likely candidate for the source of a tion at np16111, the Chukchi of diversity of haplogroup single-wave migration. In fact, the mi- Northeastern Siberia share a C3T A among Greenberg, tochondrial lineages in Siberia them- transition at np16192 with many Na- selves appear to be derived from other Dene and Eskimo samples, suggesting Turner, and Zegura’s Central East Asian populations. More- a common ancestry for members of principle Native over, population histories within Si- both language phyla.19,23 The Chukchi beria probably have disrupted genetic might be a rare Asian remnant of a American language patterning since the Americas were Beringian population that separated groupings was first colonized.25,32 The restriction to from all other Asian groups before eastern Siberia of some other Asian emergence of the transition at remarkably similar within haplogroups that exhibit low levels of np16111 and, together with the Na- each of the three diversity25 might suggest that most of Dene and Eskimo, experienced a later linguistic phyla. the present populations of that region re-expansion during which the C3T descend from a resettlement of east- transition at np16192 emerged, as ern Siberia after Beringia had already suggested by Forster and coworkers.21 been settled. Population contraction among the Central East Asian populations do remnant Beringians, who presumably Merriwether, Rothhammer, and Fer- exhibit all four lineages common in were isolated from the Amerind pop- rell,16 larger samples of haplotypes Native American populations. Popula- ulations that had earlier moved south showed near-equal levels of sequence tions in Tibet,33 Central China (desig- into North and South America, might diversity in all four lineages.24 Lorenz nated the Chinese Han),34 and Mon- have resulted in the dramatic reduc- and Smith17 found similar diversity golia20,35 carry detectable frequencies tion or extinction of members of levels in four haplogroups when geo- of haplogroups A, B, C, and D. Merri- haplogroups B, C, and D among the graphically diverse samples were con- wether and coworkers35 and Kolman, Beringians. This scenario is not con- sidered. Although some authors ques- Sambuughin, and Bermingham20 sistent with separate migrations to the tion whether the equal diversity cited Mongolia as a likely source for a New World for the Na-Dene and Eski- estimates are a result of more com- single wave of migrations. Y-chromo- 10 Evolutionary Anthropology ARTICLES some analysis of aboriginal popula- also consistent with a pre-Columbian rope, where its frequency approaches tions in South-Central Siberia near source. Though presently thought to 40%.41 In contrast to haplogroup H, Lake Baikal further support this as a be most common among speakers of haplogroup X, still the least common likely staging ground for a Beringian Algonquian languages, haplogroup X, Native American haplogroup (ϳ3% of migration.36 Of course, just as the ab- which reaches a frequency of 20% in samples screened39), is relatively rare sence of particular haplogroups from some Algonquian populations, is geo- in Europe, where it accounts for only Siberia does not mean that those hap- graphically widespread throughout approximately 3% of the samples 41 logroups were never present there, it North America among groups sharing screened. It is unlikely that admix- is entirely possible that the presence no close historic or linguistic ties.39 ture with Europeans could produce of markers elsewhere in Asia could be the wide distribution of haplogroup X Sequences consistent with haplo- the product of more recent population without also resulting in significantly group X also have been reported from movements in Asia. detectable levels of other, more com- ancient human burials in South mon European haplogroups. The high frequency of haplogroup X among Al- THE CURIOUS CASE OF gonquians and several other groups HAPLOGROUP X, A FIFTH also indicates a prehistoric presence in the New World; as such presence FOUNDING LINEAGE Y-chromosome analysis reflects the result of common ances- The identification of four haplo- of aboriginal try.39,42 groups found in Asia confirmed ear- populations in South- Analysis of ancient DNA also dem- lier evidence that Native American onstrates the presence of haplogroup populations had Asian origins. Yet in Central Siberia near X but, as yet, no other European hap- several studies of modern Native Lake Baikal further logroups in the New World before Eu- American mtDNA, certain similar se- ropean contact. CR mutations at quences appeared that did not fall into support this as a likely np16223 and np16278 have been re- one of the four known lineages.7,14 staging ground for a ported from two samples dating to Undoubtedly some of these repre- 4000 years BP and another sample sented postcontact admixture. Ward Beringian migration. Of dating to 1,000 years BP from lowland and colleagues14 reported several se- course, just as the South America.40 CR mutations con- quences sharing transitions at sistent with haplogroup X also have np16223 and np16278 that, in their absence of particular been found in two individuals from phylogenetic analysis, did not cluster haplogroups from the Norris Farms Oneota burials, a with any other Native American types. Siberia does not mean 700-year-old cemetery in west-central Torroni and coworkers7 reported that Illinois.18 Because the transitions at a small number of haplotypes found that those haplogroups np16223 and np16278 are also found in the Ojibwa shared a DdeI site loss at were never present in several mtDNA types not associated np1715, a marker also shared with a with haplogroup X, sequence data limited number of Europeans. Bailliet there, it is entirely alone do not provide incontrovertible and coworkers37 and Forster and co- possible that the evidence of the haplogroup. However, workers21 suggested that the C3Tat the Norris Farms sequences are virtu- np16278, coupled with the absence of presence of markers ally identical to those of modern Al- mutations marking haplogroups A, B, elsewhere in Asia could gonquians from the Great Lakes re- C, or D, constituted an additional hap- gion confirmed to be members of logroup. be the product of more haplogroup X.42 Malhi has also found Several lines of evidence now con- recent population individuals with both CR mutations firm haplogroup X as a fifth founding and the AccI site gain at np14465 in haplogroup in the Americas. In Brown movements in Asia. remains dated to 1340 Ϯ 40 years BP and colleagues’38 phylogenetic analy- discovered near Vantage, Washing- sis, a larger sample of Native Ameri- ton, on the Columbia Plateau. The can sequences from mtDNAs contain- haplotype of this sample included the ing the DdeI site loss at np1715 (as America.40 If the presence of these C3T transition at np16213 that well as an AccI site gain at np14465) mtDNAs were the result of recent ad- uniquely characterizes most CR se- and the transitions at np16223 and mixture with modern Europeans, quences of members of haplogroup X np16278 formed a distinct clade. Al- other European haplogroups should from the New World.43 though apparently sharing a matrilin- also be found. However, among alleg- Although haplogroup X is now ac- eal ancestor with the European hap- edly maternally full-blooded Native cepted as a pre-Columbian Native logroup X at some point deep in time, Americans, less than one-half percent American haplogroup, controversy the Native American sequences (four individuals previously classified still surrounds its origin. While the formed their own branches indepen- as “others” in a screening of more other Native American haplogroups dent of European representatives of than 800 individuals) were shown to are found in Central East Asia, haplo- haplogroup X. be members of haplogroup H,39 the group X had not, until quite recently, The distribution of haplogroup X is most common mtDNA type in Eu- been identified that far east,44 occur- ARTICLES Evolutionary Anthropology 11 ring in highest frequencies in Europe tion fragment length polymorphism ulation structure and gene pools in and Western Asia.41 This has led to the and corresponding CR mutations, in the Americas appear to have been in- hypothesis, fueled by morphometric Altaian individuals of South-Central fluenced by population expansions studies of the Kennewick Man re- Siberia.44 Haplogroup X is not as and intracontinental migrations since mains in Washington State and other common in Native Americans as are settlement.22,42,54,58 As a consequence, Paleo-Indian remains,45,46 that there the other four haplogroups. Accord- it seems unreasonable to identify any was a prehistoric migration of Euro- ingly, there is no reason to believe that extant group in the Old World, itself a peans to the New World. These re- it need ever have been common in product of many millennia of history, mains, some dated to more than 9,000 Asia in order to achieve its present as the single parent population. years BP, are morphologically distinct distribution in the Americas. It is from most modern Native American noteworthy that Y chromosome hap- HOW OLD ARE THE and Central Eastern Asian popula- lotype 1C is also found in Europe, the FIRST AMERICANS? tions. The case for repatriation of the Lake Baikal region, and the Ameri- Kennewick skeleton received consid- cas.36 Haplogroup X might once have A molecular clock, first suggested erable media attention, driven in large been present closer to Lake Baikal as by Zuckerkandl and Pauling in the part by popular accounts stating that well, and spread both east to Europe 1960s, has been employed to use mo- Kennewick man has typically Cauca- and west to the Americas in the same lecular divergence to date prehistoric soid features.47 Osteological analyses events. The rapid mutation rate and of these early Paleo-Indians actually unilateral maternal descent of mtDNA suggest closer affinities to Polynesian appear to make it particularly useful populations and the Ainu of Japan ...the popular depiction for dating events in recent prehistory. than to typical Europeans.48 They also Various estimates for the peopling of indicate that, as a group, the earliest of Kennewick Man as a the New World drawn from mtDNA Americans are also more varied than pre-Columbian data, summarized in Table 1, range modern Native American groups.49,50 broadly from about 11,000 to over While this morphological heteroge- Caucasoid in the New 40,000 years BP based on mtDNA di- neity could reflect multiple origins, it World, coupled with the vergences. This variation results in might also reflect a more generalized part from sampling haplotypes used adaptation of the earliest colonists be- discovery of haplogroup to estimate diversity and in part from fore the emergence of specialized ad- X as a founding Native variation in the methods used to cal- aptations reflected by later archaic culate molecular divergence. When traditions. Although DNA analysis did American lineage, they are presented, the standard er- not produce amplifiable ancient DNA fueled premature rors of these estimates and the range from Kennewick Man,51–53 verifiable speculation about early of the estimates themselves are rather DNA from other Paleo-Indian samples large, thus minimizing the utility of belongs to typically Native American European migrations to such measures for evaluating differ- haplogroups.54–56 Nevertheless, the the New World. Genetic ent scenarios in prehistory. It should popular depiction of Kennewick Man be noted also that these dates do not as a pre-Columbian Caucasoid in the evidence does not necessarily indicate the establishment New World, coupled with the discov- support such a of any population in the New World, ery of haplogroup X as a founding but only the separations between New Native American lineage, fueled pre- migration. World and Old World lineages, which mature speculation about early Euro- may well have begun in Asia. pean migrations to the New World.57 Archeological evidence has estab- Genetic evidence does not support lished that humans were present in such a migration. Furthermore, the migrations that spread Y chromo- North America ϳ11,500 years ago lack of other more common European some haplotype 1C before becoming when the widely distributed and well- haplogroups (or other nonmitochon- rarer still in the Baikal region. dated Clovis culture appeared. The drial genetic markers) in unadmixed The Altaians of South-Central Asia earliest known human skeletal re- Native Americans makes this scenario have been identified as one population mains date to this time. Although unlikely. outside the Americas that contains all there has long been tantalizing evi- Haplogroup X might have origi- five of the founding Native American dence of earlier occupations, little of it nated in Europe or West Asia. It is haplogroups. They may well be de- has withstood the close scrutiny nec- also possible that this haplogroup was scendants of the same source popula- essary to establish an early human once present in a Central East Asian tion that lived in Southern Siberia be- presence in the New World.59,60 Add- population that gave rise to founders fore both eastern Siberia and Beringia ing to the controversy surrounding of the New World and subsequently were colonized. However, it is highly pre-Clovis sites is the apparent lack of all but disappeared from Eastern Asia. unlikely that a single source popula- a suitable migratory route out of Ber- Some of the mystery surrounding tion has remained stable and un- ingia. While the Bering Land Bridge haplogroup X seems to have been changed over many thousands of was open throughout the last glacia- solved by the recent detection of this years. Indeed, there is substantial ev- tion, an ice-free corridor between the haplogroup, assessed by both restric- idence to the contrary. Certainly pop- Laurentide and Cordilleran ice 12 Evolutionary Anthropology ARTICLES

TABLE 1. Divergence Dates From mtDNA Data 20,000 years BP as a benchmark at a Divergence Range (Years Before Present; Error time when relatively few Native Amer- 67 Study and/or Confidence Intervals Where Reported) ican samples had been analyzed. Other estimates are based not on Torroni and co-workers, 199466 divergence from an Asian source, but A 25,862–34,091 B 11,724–15,456 instead on the accumulated diversity C 33,105–43,636 in the New World using coalescent D 18,276–24,091 theory.19,21,24 Such estimates exhibit a Schurr and co-workers, 199925 variability that in all probability is too A 26,969–35,550 large to be useful for selecting among B 13,483–17,773 alternative hypotheses regarding the C 40,972–54,009 initial peopling of the Americas.68 D 19,483–25,682 While the observed high mutation 21 Ϯ Forster and co-workers, 1996 20,180 1,000 rates in mtDNA do make them partic- (haplogroups A, B, C, and ularly useful for analyses at shallow D) Horai and co-workers, 199315 14,000–21,000 time depths such as those involving (haplogroups A, B, C, and the evolution of human populations, D) such rapid rates of change can also Brown and co-workers, 199838 12,00–17,000 or 23,000–36,000 add to the error associated with using (haplogroup X only) molecular divergence to date prehis- Stone and Stoneking, 199818 toric events. A 19k (95% CI 12k–30k) or 37k (25k–57k) It has been demonstrated that mo- B 12k (8k–21k) or 25k (16k–41k) lecular estimates do not always match C 11k (6k–21k) or 22k (13k–40k) the empirical data. A recent molecular D 15k (9k–27k) or 31k (19k–51k) analysis of modern populations hy- pothesized the presence of haplogroup V in the Basque region of Spain masses was apparently impassible continental United States via coastal by approximately 10,000 years BP from 30,000 years BP until perhaps refugia during the terminal Pleisto- based on the diversity exhibited by 11,000 years BP.61 Thus, pre-Clovis cene rather than through the ice-free modern members of this haplo- people would have to have migrated corridor.65 This, at the very least, group.69 However, subsequent analy- southward out of Beringia via the ice- raises the possibility that humans also sis of 92 ancient human remains in free corridor before 30,000 years BP. could have traveled south of the ice that region failed to confirm any signs It now appears that a 12,500 year- sheets via a similar route at this time. of this haplogroup in the region as old occupation level at Monte Verde Consequently, Monte Verde’s pre-Clo- recently as 4,000 years BP.70 This dis- in south-central Chile establishes the vis occupation lends no support to the crepancy between the molecular esti- presence of humans in the Americas hypothesis that the Americas were mates and the molecular archeologi- before Clovis.62,63 This favors a migra- colonized as early as 30,000 years BP. cal record provides no confidence in tory route to the New World other Unfortunately, this has not discour- molecular estimates of the times of than the ice-free corridor. Recent aged attempts to seek molecular evi- past events when those estimates are analysis indicates that a coastal pas- dence of an early human presence in derived solely from studies of living sage, open as early as 14,000 years BP, the Americas. Great variation in diver- populations. Unlike the case of Ra- was a likely entry point to North gence estimates among molecular mapithecus, in which molecular data America.61 Similarities in mtDNA studies results from uncertainties re- showing a later divergence of humans among populations of the west coast garding the proper calibration of mu- and the African apes led paleontolo- of North America also appear to sup- tation and divergence rates, the error gists to reconsider fossil evidence of port the hypothesis of population ex- estimates associated with these rates, an early split for the human line, mo- pansion out of Beringia associated and the events that genetic divergence lecular data suggesting an early occu- with gene flow along the west coast.64 may actually reflect. Attempts to cali- pation of the Americas have not led to On its own, this is not conclusive evi- brate a mitochondrial mutation rate discoveries of an early occupation. dence of an early coastal entry into have employed divergences dates that However, molecular evidence is still New World and, indeed, such an ex- themselves are uncertain, as is the best used as part of a holistic ap- pansion might have postdated the ear- case with the Homo-Pan split, the proach to such inquiries alongside liest migrations southward out of Ber- emergence of modern Homo sapiens, traditional archeological evidence of ingia. Nevertheless, this evidence and the linguistic break-up of the human presence. raises the possibility of such move- Chibcha language phylum.15,66 The ment and should provide fuel for ar- calculation of mutation rates has ANCIENT DNA AND THE cheological and linguistic investiga- achieved certain tautological qualities PEOPLING OF THE tions of such a claim. In addition, as well: Attempts to calculate a rate of NEW WORLD genetic data indicate that populations mtDNA sequence divergence used the of North American brown bears first peopling of the Americas, assumed to The analysis of ancient DNA in the reached the modern boundary of the have occurred between 12,000 and New World has largely confirmed the ARTICLES Evolutionary Anthropology 13

TABLE 2. Applications of mtDNA Data to Native American Nulth and Bella Coola belong.77 Migration Hypotheses Therefore, sample design probably ac- Hypotheses Regarding Migration in North America MtDNA Support counts for the lack of genetic correlation with language in this particular Athapaskan Migration to the Southwest Positive6,78 Neo-Eskimo Migration Positive87 study. Iroquian Migration Equivocal42 On a continent-wide level, Lorenz Numic Spread Positive54 and Smith6 demonstrated that Uto-Aztecan Migration and spread of Maize Negative78 mtDNA haplogroup frequency distri- Agriculture butions often do correlate with lan- Penutian Migration into California Equivocal6,64 guage or geography or both.6 In the Proto-Algonquian Migration and spread Positive42,88 north, correlations with geography were high, as were both linguistic and geographic correlations in western findings of studies of modern DNA Finally, in almost all studies of an- and other genetic polymorphism. cient Native American populations, North America. The significant levels Haplogroups A, B, C, and D have been individuals have been discovered who of correlation between language and identified through analyses of both re- do not appear to belong to one of the striction fragment length polymor- five founding lineages. In many cases, phism and CR sequencing in many this is undoubtedly a result of external prehistoric samples in both North and contamination of samples lacking It now appears that a South America.18,40,54,58,71,72 Similari- DNA or in which the DNA is inhibited 12,500 year-old ties in both haplogroup frequencies from amplifying using the polymerase and specific haplotypes from ancient chain reaction. Nonetheless, the pos- occupation level at DNA also indicate that, for the most sibility remains that additional haplo- Monte Verde in south- part, European contact did not signif- groups may be discovered by studies icantly affect mtDNA diversity in the of ancient DNA in the Americas. Such central Chile establishes Americas.18,54,72 a lineage may have either become ex- the presence of humans The presence of haplogroup X has tinct or be a yet-undiscovered lineage been confirmed in prehistoric and persisting at low levels in modern in the Americas before protohistoric burials on the Columbia populations. Clovis. This favors a Plateau,73 while sequence data sug- migratory route to the gest its presence in the prehistoric On- eota population18 and pre-Columbian POSTCOLONIZATION New World other than South America.40 Hauswirth and co- PREHISTORY WITHIN the ice-free corridor. workers74 also reported haplogroup X THE AMERICAS from Windover pond skeletons (7,000 Recent analysis to 8,000 years BP), although other se- Studies of mtDNA diversity have indicates that a coastal quences generated in the study sug- demonstrated that the multidisci- gest the possibility of contamination plinary approach that uses genetic passage, open as early in some samples. data in conjunction with cultural, ar- as 14,000 years BP, was While haplogroups B, C, and D have cheological, and linguistic patterns all been identified in Paleo-Indian can provide significant insight into a likely entry point to skeletal remains,54,55,56 the oldest re- the population prehistory of the North America. ported member of haplogroup A, the Americas (Table 2). Ward and co- most common haplogroup in North workers76 examined haplotype diver- America and the New World, dates sity within three tribes from the Pa- Ϯ 75 only to 4,504 105 years BP. How- cific Northwest region, the Nuu-Chah- mtDNA haplogroup distribution ever, relatively few Paleo-Indian sam- Nulth, the Bella Coola, and the Haida. among native North Americans sug- ples have been analyzed and a major- They concluded that these tribes gests that prehistoric population ity of these have come from the share a recent ancestry because the movements, especially in western western United States, where haplo- genetic boundaries among Native North America, were not negligible group A is rare in modern populations American groups in this region do not events. Lorenz and Smith6 also dem- except along the coast. In a prelimi- coincide with the boundaries de- nary restriction analysis of 18 samples scribed by Greenberg, Turner, and Ze- onstrated that geographic regions of dating to before 6,500 years of age, no gura11 based on language differences. North America exhibit differences in members of haplogroup A were re- However, recent re-examination of haplogroup frequency distributions. ported.56 The binomial probability of language stocks in North America Although haplogroup frequency dis- identifying no members of haplo- suggests that the Haida probably do tributions vary significantly across group A among 18 samples, given the not belong to the Na-Dene language North America, regional studies of present distribution of haplogroups family and therefore did not represent mtDNA diversity in the Northeast42 within the continental United States, a linguistic phylum that is separate and the Southwest78 have confirmed a is 0.0017. from the one to which Nuu-Chah- pattern of within-region similarities 14 Evolutionary Anthropology ARTICLES

high frequencies of haplogroups B and D have been characteristic of populations of the Columbia Plateau for at least eight millennia. In contrast, Kaestle and Smith54 have demonstrated that ancient Western Great Basin populations are statistically significantly different from modern populations in the same region, probably due to a population spread of Numic speakers into the Great Basin from southern California approximately 1,000 years BP.84 Recent regional studies of mtDNA diversity within North America have shown that detailed analyses of haplotypes can provide better evidence of ancient shared ancestry than do haplogroup frequency distributions alone, which can be similar in two populations due to chance alone. For exam- ple, Malhi, Schultz, and Smith42 have Figure 1. Map of human mitochondrion showing locations of the control region and of provided evidence from polymorphic polymorphic sites marking 5 known Native American founding haplogroups. sites in the control region of a more recent shared ancestry among speak- in haplogroup frequency distribu- evidence of unbroken ancestor and ers of Iroquoian, Caddoan, and Si- tions. In the Southwest, these similar- descendant relationships in the Amer- ouan languages than between any of ities cross-cut the boundaries among ican Southwest during the last two the three and speakers of Algonquian different unrelated languages, sug- millennia. Malhi73 has shown that languages of Eastern North Ameri- gesting considerable admixture among them. These conclusions are consistent with the results of earlier studies based on both morphology (for exam- ple, dental variation79) and blood group phenotypes.80,81 The Southeast region of North America does not dis- play a homogeneous pattern of haplogroup frequency distributions, probably due to genetic bottlenecks caused by the high impact of European contact in this region followed by genetic drift.82 Studies of ancient mtDNA diversity in most regions of North America reveal that Native American haplogroup frequency distributions often exhibit temporal as well as regional continuity.72,83 In addition to regional studies, analyses of mtDNA have been used in direct tests of specific hypotheses of population movement proposed by traditional North American prehisto- rians (archeologists and linguists) as shown in Table 2. Carlyle and col- leagues72 have demonstrated that the haplogroup frequency distribution of an ancient population that practiced the Anasazi cultural tradition in the American Southwest is not significantly different from that in modern Pueblo populations. This study pro- Figure 2. Electrophoretic gel showing PCR fragments amplified and digested to reveal vides biological as well as cultural polymorphic sites marking 5 known Native American founding haplogroups. ARTICLES Evolutionary Anthropology 15

timing of these migrations.80,81 This does not undermine the utility of genetic data, and mtDNA in particular, for future research. While our knowl- edge of the mtDNA diversity among many tribal and language groups remains limited, the growing mtDNA databases both within and outside the Americas offer a wonderful comparative tool. However, it is important to remember that mtDNA is but one marker, and one that is solely maternally inherited, and is unlikely to an- swer all questions regarding the origins of Native Americans.86 While Y-chromosome markers have been employed to address the peopling of the Americas, they have not yet been specifically used to address postcolonization events. Like mtDNA, Y-chromosome data have not on their own conclusively answered questions regarding either source populations within Asia or the number of migrations out of Asia into the New World. Clearly, nuclear markers from more populations should be examined to provide additional data relevant to Figure 3. Regional distribution of mtDNA haplogroup frequencies in North America. Adapted from Lorenz and Smith, 1996.6 these controversies, even though it is unlikely that additional data will significantly simplify what is a convo- ca.42,85 Weiss and Smith82 have shown luted and complex scenario of migra- shared mutations in the control region that suggest shared ancestry among speakers of the Muskogean languages in the Southeast, even though haplogroup frequency distributions among these groups are significantly different. Thus, while genetic boundaries do not always coincide with boundaries based on the distribution of languages and culture, the latter provide hypotheses about prehistory that can be tested using modern and prehistoric populations. It is important to note that hypotheses based on genetic evidence must be consistent with evidence derived from historical linguistic and archeological studies.

CONCLUSIONS It is not surprising that mitochondrial DNA has largely confirmed the findings of classical genetic markers regarding genetic relationships among Native American tribal groups and yet Figure 4. Alternative routes from Asia into the New World. Dotted lines represents a possible has not conclusively resolved raging path through the ice free corridor as Codilleran and Laurentide ice sheets separated. Solid debates regarding number of migra- line of arrows represents a costal route around edge using ice-free refugia along Pacific tions, source populations, and the coast. 16 Evolutionary Anthropology ARTICLES

11 Greenberg JH, Turner CGI, Zegura SL. 1986. The settlement of the Americas: a comparison of linguistic, dental and genetic evidence. Curr An- thropol 27:477–497. 12 Sapir E. 1929. Central and North American Indian languages. London: Encyclopedia Britan- nica Company, Ltd. Encyclopedia Britannica 14th ed, vol 5. p 138–141. 13 Bateman R, Goddard I, Ogrady R, Funk VA, Mooi R, Kress WJ, Cannell P. 1990. Speaking of forked tongues: the feasibility of reconciling human phylogeny and the history of language. Curr Anthropol 31:1–24. 14 Ward RH, Frazier BL, Dew-Jager K, Paabo S. 1991. Extensive mitochondrial diversity within a single Amerindian tribe. Proc Nat Acad Sci USA 88:8720–8724. 15 Horai S, Kondo R, Nakagawa-Hattori Y, Ha- yashi S, Sonoda S, Tajima K. 1993. Peopling of the Americas founded by four major lineages of mitochondrial DNA. Mol Biol Evol 10:23–47. 16 Merriwether DA, Rothhammer F, Ferrell RE. 1995. Distribution of the four founding lineage 39,41,89 Figure 5. World wide distribution of Haplogroup X frequencies. haplotypes in native Americans suggests a single wave of migration for the New World. Am J Phys Anthropol 98:411–430. 17 Lorenz JG, Smith DG. 1997. Distribution of tions and postmigrational evolution- time. Together with historical linguis- sequence variation in the mtDNA control region of native North Americans. Hum Biol 69:749– ary forces. tics, ethnographic comparisons, and 776. Although it is possible that nuclear archeological investigations, mtDNA 18 Stone AC, Stoneking M. 1998. mtDNA analy- genes may someday be more easily retains real power to illuminate pre- sis of a prehistoric Oneota population: implications for the peopling of the New World. Am J recovered from ancient human re- history. Hum Genet 62:1153–1170. mains, as of now population-level 19 Bonatto SL, Salzano FM. 1997. A single and studies of single-copy genes remain early migration for the peopling of the Americas prohibitively difficult with ancient REFERENCES supported by mitochondrial DNA sequence data. Proc Nat Acad Sci USA 94:1866–1871. DNA. The scale of the questions most 1 Wallace DC, Torroni A. 1992. American Indian 20 Kolman CJ, Sambuughin N, Bermingham E. readily addressed by ancient mtDNA prehistory as written in the mitochondrial DNA: 1996. Mitochondrial DNA analysis of mongolian is different from that of questions ad- a review. Hum Biol 64:403–416. populations and implications for the origin of New World founders. Genetics 142:1321–1334. dressed by the earliest mtDNA stud- 2 Cann RL. 2001. Genetic clues to dispersal in 21 Forster P, Harding R, Torroni A, Bandelt HJ. ies. While a decade ago research fo- human populations: retracing the past from the present. Science 291:1742–1748. 1996. Origin and evolution of native American cused on the Asian affinities and mDNA variation: a reappraisal. Am J Hum Genet 3 Anderson S, Bankier AT, Barrell BG, de Bruijn 59:935–945. principle migrations to the New MHL, Coulson AR, Drouin J, Eperon IC, Nierlich 22 Smith DG, Lorenz J, Rolfs BK, Bettinger RL, World, little light was shed upon, nor B, Roe A, Sanger F, Schrier PH, Smith AJH, Staden R, Young C. 1981. Sequence and organi- Green B, Eshleman J, Schultz B, Malhi R. 2000. interested exhibited in, postcoloniza- zation of the human mitochondrial genome. Na- Implications of the distribution of Albumin tion movements and interactions. The ture 290:457–465. Naskapi and Albumin Mexico for new world prehistory. Am J Phys Anthropol 111:557–572. sampling necessary for addressing 4 Wallace DC, Garrison K, Knowler WC. 1985. Dramatic founder effects in Amerindian mito- 23 Starikovskaya YB, Sukernik RI, Schurr TG, continent-wide phenomena is differ- chondrial DNA species. Am J Phys Anthropol Kogelnik AM, Wallace DC. 1998. mtDNA diver- ent from that necessary for character- 68:149–156. sity in Chukchi and Siberian Eskimos: implications for the genetic history of ancient Beringia izing the relationships between local 5 Schurr TG, Ballinger SW, Gan YY, Hodge JA, and the peopling of the New World. Am J Hum groups. Yet the population dynamics Merriwether DA, Lawrence DN, Knowler WC, Genet 63:1473–1491. Weiss KM, Wallace DC. 1990. Amerindian mito- at local levels have contributed to the chondrial DNAs have rare Asian mutations at 24 Bonatto SL, Salzano FM. 1997. Diversity of current genetic diversity witnessed on high frequencies, suggesting they derived from age of the four major mtDNA haplogroups, and four primary maternal lineages. Am J Hum their implications for the peopling of the New a continental scale. Identification of Genet 46:613–623. World. Am J Hum Genet 61:1413–1423. such population dynamics can con- 6 Lorenz JG, Smith DG. 1996. Distribution of 25 Schurr TG, Sukernik RI, Starikovskaya YB, tribute significantly to our under- four founding mtDNA haplogroups among Na- Wallace DC. 1999. Mitochondrial DNA variation in Koryaks and Itel’men: population replacement standing of the broader questions per- tive North Americans. Am J Phys Anthropol 101: 307–323. in the Okhotsk Sea-Bering Sea region during the Neolithic. Am J Phys Anthropol 108:1–39. taining to the settlement of the New 7 Torroni A, Schurr TG, Cabell MF, Brown MD, World. Further, while critics of an- Neel JV, Larsen M, Smith DG, Vullo CM, Wallace 26 Excoffier L, Langaney A. 1989. Origin and differentiation of human mitochondrial DNA. cient DNA may charge that small sam- DC. 1993. Asian affinities and continental radia- tion of the four founding Native American Am J Hum Genet 44:73–85. ples limit the power of the conclu- mtDNAs. Am J Hum Genet 53:563–590. 27 Szathmary EJE. 1993. mtDNA and the peo- sions drawn, ancient DNA remains 8 Nichols J. 1990. Linguistic diversity and the 1st pling of the Americas (editorial). Am J Hum the only direct way of detecting tem- settlement of the New World. Language 66:475– Genet 53:793–799. 28 Templeton AR. 1998. Human races: a genetic poral change in the genetic composi- 521. 9 Rogers RA, Martin LD, Nicklas TD. 1990. Ice- and evolutionary perspective. Am Anthropol 100: tion of a population. MtDNA should Age geography and the distribution of native 632–650. be seen as another tool with which to North American languages. J Biogeogr 17:131– 29 Shields GF, Hecker K, Voevoda MI, Reed JK. formulate and test hypotheses about 143. 1992. Absence of the Asian-specific region V mi- 10 Nettle D. 1998. Explaining global patterns of tochondrial marker in native Beringians. Am J demic events such as migrations, ex- language diversity. J Anthropol Archaeol 17:354– Hum Genet 50:758–765. pansions, and continuity through 374. 30 Torroni A, Sukernik RI, Schurr TG, Starik- ARTICLES Evolutionary Anthropology 17 ovskaya YB, Cabell MF, Crawford MH, Comuzzie 48 Powell JF, Rose JC. 1999. Report on the non- Rate of sequence divergence estimated from re- AG, Wallace DC. 1993. mtDNA variation of ab- destructive examination, description, and analy- striction maps of mitochondrial DNAs from original Siberians reveals distinct genetic affini- sis of the human remains from Columbia Park, Papua New Guinea Cold Spring Harbor Symp ties with Native Americans. Am J Hum Genet Kennewick, Washington: report on the osteolog- Quant Biol 51(Part I):433–439. 53:591–608. ical assessment of the “Kennewick Man” skeleton 68 Tavare S, Balding DJ, Griffiths RC, Donnelly 31 Yao YG, Watkins WAS, Zhang YP. 2000. Evo- (CENWW.97.Kennewick). Chapter 2: National P. 1997. Inferring coalescence times from DNA lutionary history of the mtDNA 9-bp deletion in Park Service. sequence data. Genetics 145:505–518. Chinese populations and its relevance to the peo- 49 Powell JF, Neves WA. 1999. Craniofacial mor- 69 Torroni A, Bandelt HJ, D’Urbano L, Lahermo pling of east and southeast Asia. Hum Genet phology of the first Americans: pattern and pro- P, Moral P, Sellitto D, Rengo C, Forster P, Savon- 107:504–512. cess in the peopling of the New World. Yearbook taus ML, Bonne-Tamir B, Scozzari R. 1998. 32 Crawford MH, Williams JT, Duggirala R. Phys Anthropol 110, Supp 29:153–188. mtDNA analysis reveals a major late Paleolithic 1997. Genetic structure of the indigenous popu- 50 Neves WA, Munford D, do Carmo Zanini M, population expansion from southwestern to lations of Siberia. Am J Phys Anthropol 104:177– Pucciarelli HM. 1999. Cranial morphological northeastern Europe. Am J Hum Genet 62:1137– 192. variation in South America and the colonization 1152. of the New World: towards a four migration 33 Torroni A, Miller JA, Moore LG, Zamudio S, 70 Izagirre N, de la Rua C. 1999. An mtDNA model? Ciencia e Cultura (Sao Paulo) 51:151– Zhuang J, Droma T, Wallace DC. 1994. Mito- analysis in ancient Basque populations: implica- 165. chondrial DNA analysis in Tibet: implications for tions for haplogroup V as a marker for a major the origin of the Tibetan population and its ad- 51 Smith DG, Malhi R, Eshleman JA, Kaestle FA. Paleolithic expansion from Southwestern Eu- aptation to high altitude. Am J Phys Anthropol 2000. Report on DNA analysis of the remains of rope. Am J Hum Genet 65:199–207. “Kennewick Man” from Columbia Park, Wash- 93:189–199. 71 Lalueza C, Perez-Perez A, Prats E, Cornudella ington: National Park Service. 34 Ballinger SW, Schurr TG, Torroni A, Gan YY, L, Turbon D. 1997. Lack of founding Amerindian Hodge JA, Hassan K, Chen KH, Wallace DC. 52 Kaestle FA. 2000. Report on DNA analysis of mitochondrial DNA lineages in extinct aborigi- 1992. Southeast Asian mitochondrial DNA anal- the remains of “Kennewick Man” from Columbia nes from Tierra del Fuego-Patagonia. Hum Mol ysis reveals genetic continuity of ancient Mongol- Park, Washington: Nation Park Service. Genet 6:41–46. oid migrations. Genetics 130:139–152. 53 Merriwether DA, Cabana GS. 2000. Ken- 72 Carlyle SW, Parr RL, Hayes MG, O’Rourke 35 Merriwether DA, Hall WW, Vahlne A, Ferrell newick Man ancient DNA analysis: final report DH. 2000. Context of maternal lineages in the RE. 1996. MtDNA variation indicates Mongolia submitted to the Department of the Interior: Na- Greater Southwest. Am J Phys Anthropol 113:85– may have been the source for the founding pop- tional Park Service. 101. ulation for the New World. Am J Hum Genet 54 Kaestle FA, Smith DG. 2001. Ancient mito- 73 Malhi RS. 2001. Investigating prehistoric 59:204–212. chondrial DNA evidence for prehistoric popula- population movements in North America with tion movement: the Numbic expansion. Am J 36 Karafet TM, Zegura SL, Posukh O, Osipova L, ancient and modern mtDNA. University of Cali- Phys Anthropol 115:1–12. Bergen A, Long J, Goldman D, Klitz W, Harihara fornia, Davis. Doctoral dissertation, Dept. of An- S, de Knijff P, Wiebe V, Griffiths RC, Templeton 55 Stone AC, Stoneking M. 1996. Genetic analy- thropology. AR, Hammer MF. 1999. Ancestral Asian sourc- ses of an 8000 year-old Native American skele- 74 Hauswirth WW, Dickel CD, Rowold DJ, e(s) of New World Y-chromosome founder hap- ton. Ancient Biomolecules 1:83–87. lotypes. Am J Hum Genet 64:817–831. Hauswirth MA. 1994. Inter- and intrapopulation 56 Smith DG, Malhi RS, Eshleman JA, Kaestle studies of ancient humans. Experientia (Basel) 37 Bailliet G, Rothhammer F, Carnese FR, Bravi FA. 2002. Mitochondrial DNA haplogroups of Pa- 50:585–591. CM, Bianchi NO. 1994. Founder mitochondrial leoamericans in North America. In: Bonnichsen haplotypes in Amerindian populations. Am J R, Gruhn R, Steele DG, Stanford D, Lepper B, 75 Kaestle FA. 1998. Molecular evidence for pre- Hum Genet 55:27–33. Warren CN editors. Beyond Clovis: where we historic Native American population movement: the numic expansion. University of California, 38 Brown MD, Hosseini SH, Torroni A, Bandelt have been, where we are, and where we are go- ing. College Station, TX: TexasA&MUniversity Davis. Doctoral dissertation, Dept. of Anthropol- H-J, Allen JC, Schurr TG, Scozzari R, Cruciani F, ogy. Wallace DC. 1998. mtDNA haplogroup X: an an- Press. cient link between Europe/Western Asia and 57 Morell V. 1998. Human genetics: genes may 76 Ward RH, Redd A, Valencia D, Frazier B, North America? Am J Hum Genet 63:1852–1861. link ancient Eurasians, Native Americans. Sci- Paabo S. 1993. Genetic and linguistic differentiation in the Americas. Proc Nat Acad Sci USA 39 Smith DG, Malhi RS, Eshleman J, Lorenz JG, ence 280:520–520. 90:10663–10667. Kaestle FA. 1999. Distribution of mtDNA haplo- 58 Parr RL, Carlyle SW, O’Rourke DH. 1996. An- group X among Native North Americans. Am J cient DNA analysis of Fremont Amerindians of 77 Campbell I. 1997. American Indian languag- Phys Anthropol 110:271–284. the Great Salt Lake Wetlands. Am J Phys An- es: the historical linguistics of Native America. New York: Oxford University Press. 40 Ribeiro-Dos-Santos AKC, Santos SEB, thropol 99:507–518. Machado AL, Guapindaia V, Zago MA. 1996. 59 Meltzer DJ. 1993. Pleistocene peopling of the 78 Malhi RS, Mortensen HM, Eshleman JA, Heterogeneity of mitochondrial DNA haplotypes Americas. Evol Anthropol 1:157–169. Lorenz JG, Kaestle FA, Johnson JR, Gorodezky in Pre-Columbian natives of the Amazon region. 60 Dixon EJ. 2001. Human colonization of the C, Smith DG. 2002. Native American mtDNA in Am J Phys Anthropol 101:29–37. Americas: timing, technology and process. Qua- the American Southwest. Am J Phys Anthropol, in press. 41 Torroni A, Huoponen K, Francalacci P, ternary Sci Rev 20:277–299. Petrozzi M, Morelli L, Scozzari R, Obinu D, 61 Mandryk CAS, Josenhans H, Fedje DW, 79 Turner CGI. 1993. Southwest Indian teeth: Savontaus ML, Wallace DC. 1996. Classification Mathewes RW. 2001. Late Quaternary paleoen- Southwest Indians: Prehistory through dentition. of European mtDNAs from an analysis of three vironments of Northwestern North America: im- Res Exploration 9:32–53. European populations. Genetics 144:1835–1850. plications for inland versus coastal migration 80 Brown KS, Hanna BL, Dahlberg AA, Strand- 42 Malhi RS, Schultz BA, Smith DG. 2001. Dis- routes. Quaternary Sci Rev 20:301–314. skov HH. 1958. The distribution of blood group tribution of mitochondrial DNA lineages among 62 Dillehay TD. 1997. Monte Verde: a Late Pleis- alleles among Indians of Southwest North Amer- native American tribes of northeastern North tocene settlement in Chile, vol. 2: The archaeo- ica. Am J Hum Genet 10:175–195. America. Hum Biol 73:17–55. logical context. Washington, D.C.: Smithsonian 81 Spuhler JN. 1979. Genetic distances, trees 43 Malhi RS, Smith DG. 2002. Brief communi- Institution Press. and maps of North American Indians. In: Laugh- cation: haplogroup X confirmed in prehistoric 63 Dillehay TD. 1999. The Late Pleistocene cul- lin WAS, Harper AB, editors. The first Americans: North America. Am J Phys Anthropol 119:84–86. tures of South America. Evol Anthropol 7:206– origins, affinities, and adaptations. New York: 44 Derenko MV, Grzybowski T, Malyarchuk BA, 216. Gustav Fischer. p 135–184. Czarny J, Miscicka-Sliwka D, Zakharov IA. 2001. 64 Eshleman JA. 2002. Mitochondrial DNA and 82 Weiss DA, Smith DG. n.d. Evidence for a re- The presence of Mitochondrial haplogroup X in prehistoric population movements in Western cent mtDNA bottleneck among Native Americans Altaians from South Siberia. Am J Hum Genet North America. University of California, Davis. from the Southeastern United States. Submitted. 69:237–241. Doctoral dissertation, Dept. of Anthropology. Am J Phys Anthropol. 45 Jantz RL, Owsley DW. 2001. Variation among 65 Leonard JA, Wayne RK, Cooper A. 2000. Pop- 83 O’Rourke DH, Hayes MG, Carlyle SW. 2000. early North American crania. Am J Phys An- ulation genetics of ice age brown bears. Proc Nat Spatial and temporal stability of mtDNA haplo- thropol 114:146–155. Acad Sci USA 97:1651–1654. group frequencies in native North America. Hum 46 Steele DG, Powell JF. 1997. Biological affini- 66 Torroni A, Neel JV, Barrantes R, Schurr TG, Biol 72:15–34. ties of the oldest recovered North Americans: the Wallace DC. 1994. Mitochondrial DNA “clock” 84 Bettinger RL, Baumhoff MA. 1982. The Nu- Spirit Cave and Pyramid Lakes data. Am J Phys for the Amerinds and its implications for timing mic spread: Great Basin cultures in competition. Anthropol Supplement 24:218. their entry into North America. Proc Nat Acad Am Antiquity 47:485–503. 47 Preston D. 1997. The lost man. The New Sci USA 91:1158–1162. 85 Chafe WL. 1976. The Caddoan, Iroquoian and Yorker, June 16, 1997 p. 70. 67 Stoneking M, Bhatia K, Wilson AC. 1986. Siouan languages. The Hague: Mouton. 18 Evolutionary Anthropology ARTICLES

86 Szathmary EJE. 1993. Genetics of aboriginal ing the Proto-Algonquian migration: analysis of berhiwot T, Moisan JP, Khunsnutdinova E, Os- North Americans. Evol Anthropol 1:202–220. mtDNA. Papers of the 32nd Algonquian Conference. sipova L, Stepanov V, Torroni A, Rickards O, 87 Hayes MG, O’Rourke DH. 2001. Genetic sig- Manitoba: University of Manitoba Press. p 470–492. DeStefano GF, Papiha S, Beckman L, Rudan P, natures of migrations and population replace- 89 Reidla M, Kivisild T, Metspalu E, Kaldma K, Angnou NP, Koziel S, Usanga E, Villems R. 2002. ments during human colonization of the North Tambets K, Tolk H-V, Parik J, Bermisheva M, Early postglacial spread of haplogroup X from American Arctic. Am J Hum Genet 69:179. Zhadanov S, Pennarun E, Gubina M, Gol- Eurasia to America. In Preparation. © 2003 Wiley-Liss, Inc. 88 Schultz BA, Malhi RS, Smith DG. 2001. Examin- ubenko M, Damba L, Fedorova S, Gusar V, Ge-

Forthcoming Special Issue Cultural Evolution in Primates Edited by Charles Janson and Eric Alden Smith

Contributions Include: • An Overview of Primate Traditions Dorothy Fragaszy • Traditions in Monkeys Susan Perry and Joseph H. Manson • Cultural Panthropology Andrew Whiten • Is Culture a Golden Barrier Between Human and Chimpanzee? Christophe Boesch • The Adaptive Nature of Culture Michael Alvard • Cultural Evolution and the New Old Archaeology Marta Mirazo´ n Lahr and Robert Foley