* Department of Anthropology, University of Arizona
Division of Biotechnology, University of Arizona
Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia
Institute of Cytology and Genetics, Novosibirsk, Russia
Correspondence: E-mail: mfh{at}u.arizona.edu.
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Abstract |
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Key Words: Native Americans Y chromosome SNPs and STRs divergence dates single migration Altai Mountains
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Introduction |
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The last major human continental colonization episode, the settlement of the Americas, is a topic of intense interest and controversy for researchers in numerous scientific fields, including genetics. In 1986 Greenberg, Turner, and Zegura published a widely cited, synthetic, position paper on the early peopling of the Americas that stressed the apparent congruence of the then available data from linguistics, dental morphology, and traditional biparental nuclear genetic systems within the context of the archaeological record. Their major explanatory hypothesis, the "three-wave" or "tripartite" model, was based on the proposition that all indigenous Native American populations could be allocated to three distinct linguistically defined groups (i.e., Amerind, Na-Dene, and Aleut-Eskimo) that had their origins in three chronologically separate migrations from different geographic areas of Asia (Greenberg, Turner, and Zegura 1986). Although a large number of studies from diverse disciplines have subsequently explored the issues raised in their highly controversial paper, unsolved problems today still include the number and timing of early migration(s) to the Americas, the geographic location of the source populations(s), and the evolutionary processes that have interacted to sculpt the Native American gene pool (Zegura 2002). Our present contribution seeks to provide a more fine-grained paternal genetics perspective for the eventual resolution of these important questions than either our earlier attempts (Karafet et al. 1997, 1999) or those of other research groups (Lell et al. 1997, 2002; Santos et al. 1999; Underhill et al. 1996).
The first two human Y chromosome marker studies appeared in 1985 (Casanova et al. 1985; Lucotte and Ngo 1985). It was not until almost a decade later that Torroni and co-workers (1994a) published the first Y chromosome data on Native Americans. Numerous surveys of variation on the non-recombining portion of the Y chromosome (NRY) devoted primarily to Amerind speakers quickly followed (Pena et al. 1995; Santos et al. 1995, 1996; Underhill et al. 1996; Bianchi et al. 1997; Karafet et al. 1997; Lell et al. 1997). These early data were generally interpreted to support a single-origin (and one-wave) model for the members of Greenberg's (1987) three major New World linguistic groups, despite occasional sampling problems wherein one or more of these linguistic groups lacked representation.
Karafet et al. (1999) investigated four migration models for the early paternal peopling of the Americas and presented a visual portrayal of these various models along with their hypothesis as to the geographic source of Native American Y chromosomes, shown as a circle that included the following territory: Lake Baikal (eastward to the Trans-Baikal and southward into northern Mongolia), the Lena River headwaters, the Angara and Yenisey river basins, the Altai Mountain foothills, and the region south of the Sayan Mountains (including Tuva and western Mongolia). Although both of their proposed major Y chromosome American founding lineages could be traced to possible ultimate dispersal sources within this circle, the authors favored a two-migration scenario, a proposal that has recently been supported by Lell et al. (2002) based on their Y chromosome data. Unfortunately, relatively secure dates for the two migrations (or for the single-migration scenario) based on Y chromosome microsatellites have not been published.
Thus, the major purposes of the present article are to (1) use a larger Y chromosome database that includes many more microsatellite and single-nucleotide polymorphism markers to refine our previous analyses (Karafet et al. 1997, 1999) of founder versus admixture-derived lineages in the Americas; (2) narrow down the most probable area of the postulated Asian geographic source of Native American Y chromosomes; (3) estimate the time of divergence between the Native American population system(s) and various Asian population systems; and (4) address the most likely number of migrations detected so far by Y chromosome data from Native Americans.
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Subjects and Methods |
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For the microsatellite analysis 10 STRs (DYS19, DYS388, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393, DYS426, and DYS439) were typed in two multiplex PCR reactions. Primer sequences were published in Kayser et al. (1997) and Redd et al. (2002), and PCR conditions were given by Redd et al. (2002). The PCR product was electrophoresed on a 3100 Genetic Analyzer (Applied Biosystems) with a 36 cm array and filter set D. The data were analyzed with Genescan (v. 3.7, Applied Biosystems) and Genotyper (v. 1.1, Applied Biosystems). For all statistical analyses DYS389I was subtracted from DYS389II because the DYS389II PCR product also contains DYS389I.
Terminology
We follow the terminological conventions recommended by the Y Chromosome Consortium (YCC 2002) for naming NRY lineages. Capital letters AR identify the 18 major Y chromosome clades or haplogroups. Lineages not defined on the basis of a derived character state represent interior nodes of the tree and are potentially paraphyletic. Thus, the term paragroup (rather than haplogroup) is used to describe these lineages and these paragroups are distinguished by the * (asterisk) symbol. For the sake of simplicity, we will refer to paragroups as haplogroups throughout the text. Lineages excluded from a haplogroup are listed in table 2 after an initial "x" symbol within parentheses, after the haplogroup name for the official lineage-based naming system. We opted to omit the "x" notation and parenthetical convention for the short-hand mutation-based names used throughout the text. When no farther downstream markers in the YCC 2002 tree were typed for this study, we considered the most derived typed marker to represent a haplogroup. Table 2 gives a complete list of the lineage-based and mutation-based names of the 42 haplogroups found in this study (Karafet et al. 2002). As suggested by de Knijff (2000), distinct Y chromosomes identified by STRs are designated "haplotypes."
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Results |
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Y Chromosome Diversity
The number of haplogroups in the various Native American populations ranged from 1 in the monomorphic Mixe and Kuna to 11 in the Sioux. Although only 17 haplogroups were found in Native Americans, the much smaller Central Asian sample contained 30 different haplogroups (table 1). The mean number of pairwise differences among haplogroups (p) ranged from 0, again in the Mixe and Kuna, to 5.47 in the Tanana, with an overall Native American value of 2.64. The corresponding Asian p values ranged from 3.40 in South Asia to 5.15 in Central Asia. Both SNP diversity measures exhibit the same pattern: on average Native American Y chromosome diversity is much reduced when compared with Asian diversity. For the microsatellite data, the mean number of pairwise differences also indicates a moderate reduction in genetic diversity for the Native Americans (5.13) compared with Asian values ranging from 5.66 in Southeast Asia to 6.10 in Central Asia (data not shown).
The STR data reflect a general reduction in number of haplotypes and variance in repeat number for the Native American data compared with the Asian data (table 1). The variance in repeat number value for Native Americans was 0.61, whereas the Asian variances ranged from 0.75 in Southeast Asia to 1.03 in East Asia (table 1). Thus, the overall trend in the STR data is, once again, toward a reduction in genetic diversity/variation for the Native American data set.
Median-Joining Microsatellite Networks
Figure 3 displays a median-joining network (Bandelt, Forster, and Rohl 1999) for haplogroup Q-P36* in Asia and the Americas, noting the position of the Q-M3 lineage (see cross-hatch). The ancestral node leading to Q-M3 has haplotype (DYS19 = 13; DYS388 = 12; DYS389I = 13; DYS389II = 30; DYS390 = 23; DYS391 = 10; DYS392 = 14; DYS393 = 13; DYS426 = 12; and DYS439 = 12) and was present in 3 Altai, 1 Ket, and 1 Selkup. The vast majority of the close neighbors of this node were also confined to the Altai, Ket, and Selkup populations.
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Discussion |
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Our diversity results (table 1) also underscore the potential role of genetic drift on the Native American population system. Both SNP diversity measures showed a reduction in Native American paternal genetic diversity compared with values from Asian populations. Likewise, the overall trend in the STR data was toward a reduction in genetic diversity/variation for the Native American system, although to a lesser degree.
Asian Source Region
Earlier studies based on a much smaller number of markers led to the hypothesis of a Central Asian/South Siberian source for Native American Y chromosomes (Karafet et al. 1999; Santos et al. 1999). Our new SNP and microsatellite data have the potential to permit a finer geographic resolution than was previously possible. Both Native American founder haplogroups are present at moderately high frequencies in our sample of 98 southern Altai (Q = 17%; C = 22%); however, it is the STR data that proved to be of critical import for narrowing down the presumptive Asian source region. The ancestral nodes leading to both Q-M3 (fig. 3) and C-P39 (fig. 4), the two Native Americanspecific haplogroups, were present in the southern Altai individuals. Although the Kets and Sekups currently inhabit the eastern part of Western Siberia and the Yenisey River Valley, according to Russian ethnographers, their ancient homelands are thought to lie farther south, on the slopes of the Sayan and Altai mountains (Popov and Dolgikh 1964; Prokof'yeva 1964; Karafet et al. 1999). Thus, our present data support the hypothesis that the Altai Mountain region is the principal candidate for the geographic source of the founding Native American Y chromosomes.
This hypothesis is concordant with the recent results of Derenko et al. (2000, 2001), involving a candidate Asian source region for all five major Native American mtDNA founder haplogroups (i.e., haplogroups A, B, C, D, and X). Until their 2001 report, the enigmatic minor founder lineage, haplogroup X, had never been discovered anywhere in East, Central, or North Asia, although it is present in both Europeans and Native Americans. Derenko et al. (2001) found that not only did both northern and southern Altaians have haplogroups A, B, C, and D, but 3.5% of the 202 Altai surveyed were actually haplogroup X. It should be noted, however, that all of our Altai Y chromosomes were derived from southern Altai populations and represent different samples than those used in the Derenko et al. (2001) study. Also, the Altaian haplogroup X mtDNAs are not identical to Native American haplogroup X mtDNAs (Derenko et al. 2001). Nevertheless, as far as we are aware, only the Altai region possesses all of the major Native American Y chromosome and mtDNA founding haplogroups, thereby making it the best available candidate for the ancestral source region for the Native American population system. As a caveat, we must note that it is, of course, possible that a population moved into the Altai Mountain region (presumably from the southwest) and that part of this population remained in the vicinity of the Altai and Sayan Mountains while their relatives continued moving to the northeast, eventually crossing Beringia to the Americas after the Last Glacial Maximum. In fact, by running the arrow of time backward to 100,000 years ago, all Native Americans can ultimately be traced to a dispersal from Africa; however, our main intent was to try to locate those Asian populations that are genetically the closest paternal relatives of Native Americans and who may have shared a common source with today's Native American population system. Unfortunately, without numerous chronologically secure and geographically appropriate ancient DNA samples, we may never be able to prove conclusively that modern Native Americans actually came from the Altai Mountains.
Timing of Entry into the Americas
A variety of genetic dating techniques, including mutational ages, mismatch distribution expansion dates, coalescence ages, and population divergence dates, have been employed to estimate the date of colonization. Cavalli-Sforza, Menozzi, and Piazza (1994) used autosomal data as a basis for their estimate of 32,000 years ago for the divergence of the Native American population system. Stone and Stoneking (1998) discussed a number of studies based on mtDNA that favored colonization dates before 20,000 BP and presented their own evidence for a 23,00037,000 population expansion. Although mtDNA haplogroup lineages A, C, and D have generally yielded dates earlier than 20,000 BP, Schurr (2000) gave a restriction fragment length polymorphism (RFLP)-derived date of 17,70013,500 years ago for haplogroup B, an estimate consistent with the earlier claims of Torroni et al. (1994b) and Wallace (1997) that haplogroup B in the Americas was considerably younger than the other three lineages. A possible dispersal from Eurasia to the Americas has also been dated based on haplogroup X. Brown et al. (1998) proposed that this range expansion took place either between 36,000 and 23,000 BP or 17,000 and 12,000 BP.
Earlier dating attempts using Y chromosome data have lacked precision. For instance, the origin of the Q-M3 Native Americanspecific lineage has been dated at either 30,000 years ago or as recently as 2,100 years ago (Underhill et al. 1996), 11,0009,000 years ago (Ruiz-Linares et al. 1999), 7,650 ± 5,000 years BP (Karafet et al. 1999), and 5,820 ± 2,330 years BP (Karafet, unpublished data). The mutational age of Q-P36*, the marker defining the entire Q lineage, is 17,700 ± 4,820 years BP (Hammer and Zegura 2002), whereas age estimates for the entire C lineage and the Native American-specific C-P39 are 27,500 ± 10,100 and 2,550 ± 1910 years BP, respectively (Hammer and Zegura 2002; Karafet, unpublished data). Bianchi et al. (1998) estimated that their major founder compound haplotype (based on Q-M3, a Y-specific alphoid system, and 7 microsatellites) had an average age of 22,770 years.
In contrast, all of our divergence time estimates range from 10,100 to 17,200 years ago irrespective of statistical method, population comparison, or haplogroup employed, and standard errors range from 3,200 to 6,000 years (table 3). Especially noteworthy is the general lack of temporal separation between the divergence dates based on the Q and C lineages, with only the Upper Bound TD date hinting at an earlier separation for the Q lineage. Our divergence dates are most compatible with the late entry (<20,000 BP) school championed by most American archaeologists (Meltzer 1993, 1997; West 1996; Fiedel 2000). Indeed, the earliest generally accepted archaeological site in the Americas is Monte Verde, Chile, at 14,500 years BP (calibrated) (Meltzer 1997), and there are no securely dated skeletal remains older than 12,000 years BP (uncalibrated) anywhere in the Americas (Powell and Neves 1999; Zegura 2002). It should also be remembered that genetic evidence is expected to provide maximum age estimates for the peopling of the Americas, whereas archaeology only provides minimum estimates (unless we are fortunate enough to find the very first site in the Americas; Meltzer 2004). Likewise, Nettle's (1999) recent language-based analysis argues for a 13,00014,000 BP entry date. In sum, the paternal genetic data lead to the conclusion that a relatively late entry date is more likely than the mtDNA-based early entry (>20,000 years ago) scenario. Moreover, mtDNA lineage expansions could have taken place in Asia rather than the Americas (Stone and Stoneking 1998), and it should be remembered that polymorphism (caused by a new mutation) generally precedes polytypy (i.e., population divergence) in evolution (Pamilo and Nei 1988), so that many of the proposed early colonization dates may not, in fact, date the population divergence associated with the actual formation of the Native American population system.
Number of Migrations
Only the synthetic work on traditional serogenetic and protein-coding loci by Cavalli-Sforza, Menozzi, and Piazza (1994) and some of the early mtDNA work (Torroni et al. 1992) have supported the Greenberg, Turner, and Zegura (1986) tripartite model. At present, the preferred explanation for many mtDNA workers is a single migration (Merriwether, Rothhammer, and Ferrell 1995; Kolman, Sambuughin, and Bermingham 1996; Bonatto and Salzano 1997a, 1997b; Stone and Stoneking 1998), although a four-migration scheme is preferred by Torroni et al. (1994a, 1994b) and Wallace (1997), also based on mtDNA data. In fact, numerous independent data sets from linguistics (Nichols 1994/1995), immunology (Schanfield 1992), skeletal biology (Neves et al. 1999), and archaeology (Roosevelt et al. 1996) have been interpreted to support a four-migration model, often by grafting an earlier Pre-Clovis entry onto the Greenberg, Turner, and Zegura (1986) scenario (Neves and Pucciarelli 1991; Powell and Neves 1999; Zegura 2002). As mentioned earlier, the initial Y chromosome data led to a single-origin model (Pena et al. 1995; Santos et al. 1995, 1996, 1999; Underhill et al. 1996; Bianchi et al. 1997; Karafet et al. 1997; Lell et al. 1997), whereas later studies supported a two-wave model (Karafet et al. 1999; Lell et al. 2002), and Forster et al. (1996) presented a single-migration (followed by a re-expansion) model based on mtDNA evidence that can be interpreted as a two-wave scenario.
Our new data and analyses are most consistent with the single-migration alternative. For instance, (1) the divergence dates for the Q and C lineages were generally quite similar (table 3), (2) both of these lineages seem to have originated in the Altai Mountain region (figs. 3 and 4), (3) the AMOVA CT values for Greenberg's three linguistic groups were not statistically significant (table 4), (4) and genetics and language were uncorrelated in Mantel tests. Therefore, we have no compelling data that would refute Laughlin's (1986: 490) contention that a "single small migration some 16,000 years ago appears most parsimonious."
Thus, despite distributional differences for the Q and C lineages on both sides of the Bering Strait (Karafet et al. 1999, 2002), we cannot dismiss the parsimonious conjecture that the initial founding population possessed both lineages with somewhat unequal frequencies, and that these initial frequency differences were increased through time by successive episodes of intragenerational and intergenerational genetic drift. Subsequently, this single polymorphic Beringian population became subdivided geographically and linguistically (Szathmary 1993). This scenario is concordant with theoretical expectation for a population fragment event (Knowles and Maddison 2002). Moreover, it is consistent with the population fragmentation signal between Asia and the Americas detected in mtDNA data by Templeton (1998, 2002).
Admixture and Haplogroup R
The combination of new haplogroup and microsatellite data from haploid systems with phylogeographic information allows inferences about admixture that can resolve earlier controversies in the literature. For instance, Lell et al. (2002) and Lell, Sukernik, and Wallace (2002) proposed a two-migration model wherein an unresolved lineage, equivalent to haplogroup R, joined haplogroup C as chief binary polymorphism markers for their second migration, which they derived from the Lower Amur River/Sea of Okhotsk region. Their earlier migration supposedly brought the Q lineage to the Americas from southern Middle Siberia. Four microsatellite markers were also used to characterize these two hypothesized migrations. Tarazona-Santos and Santos (2002) questioned the validity of Lell et al.'s (2002) second migration and proposed that the presence of what are now known to be haplogroup R individuals in the Americas was due to admixture.
On the basis of our new data and analyses, 76 of 79 Native American R lineage chromosomes belong to haplogroup R-P25. The median-joining network for R-P25 (fig. 5) exhibits extensive sharing of microsatellite haplotypes between Europeans and Native Americans, unlike the case for Asians. Also, the European and Native American modal haplotypes are identical for haplogroup R-P25, whereas the Asian modal haplotype differs at two positions. To investigate the hypothesis of EuropeanNative American admixture for haplogroup R-P25 further, we performed a 16-population non-metric multidimensional scaling (MDS) analysis on the R-P25 microsatellite data (data not shown). The five European populations formed a distinct cluster with five of the seven Native American groups. In contrast, none of the four Asian populations were part of the EuropeanNative American cluster.
In sum, our evidence supports the admixture hypothesis for the presence of R-P25 individuals in Native American populations and concurs with the recent findings of Bosch et al. (2003), who concluded that all 18 of their haplogroup R Greenlandic Inuit (n = 69) are the result of European admixture. Their overall admixture estimate for their Greenlandic Inuit sample was 58 ± 6% and they conjectured that the Greenlandic Inuit sample in Karafet et al. (1999) from Nanortalik (n = 62), one of their minor sampling locations (n = 5), exhibited between 15% and 56% European admixture, depending on the outcome of further typing to resolve haplogroup status according to the YCC (2002) system. Our new results yielded an admixture estimate of 17% ± 5% for this Inuit (i.e., Aleut-Eskimospeaking) sample, whereas the admixture estimate for our entire Native American sample was 17% ± 2%, following the procedures in Bosch et al. (2003).
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Summary |
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Acknowledgements |
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Footnotes |
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