*Department of Evolutionary Biology, Tartu University and Estonian Biocentre, Estonia;
Department of Medical Genetics, Sun Yat-Sen University of Medical Sciences, People's Republic of China;
Department of Human Genetics, University of Newcastle-upon-Tyne;
Department of Mathematics, University of Hamburg, Germany
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Abstract |
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Introduction |
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In contrast to West Eurasia (Macaulay et al. 1999b
), the Americas (Torroni et al. 1993a;
Brown et al. 1998
), and Siberia (Torroni et al. 1993b;
Schurr et al. 1999
), the mitochondria of East Asia (Japan, in particular) have not yet been classified satisfactorily. Eurasian mtDNAs belong to two superhaplogroups ("trunks") M (Chen et al. 1995
) and N (first defined in fig. 3 of Quintana-Murci et al. 1999
by one of its characteristic mutations and then baptized in fig. 2 of Alves-Silva et al. 2000
), which differ at nucleotide position (np) 10400 (and further coding region sites). These trunks encompass the known Asian-specific haplogroups C, D, E, G, Z ("limbs" and "boughs" of the M "trunk") and A, B, F, Y (limbs and boughs of the N trunk). Although high-resolution restriction fragment length polymorphisms (RFLPs) define all these haplogroups unambiguously except for Z (Starikovskaya et al. 1998
; Schurr et al. 1999
), their branching order within M and N, respectively, remained undetermined. Moreover, the nine haplogroups do not quite cover all East Asian mtDNAs, and toward the periphery of the mtDNA tree, potentially region-specific boughs and "twigs" that may be recognized by certain hypervariable segments (HVS)-I motifs in conjunction with single coding region sites still await full description.
We have therefore used hitherto nonsynthesized information concerning Asian complete mtDNA sequences (Yoneda et al. 1990
; Ozawa et al. 1991
; Jun, Brown, and Wallace 1994
; Ikebe, Tanaka, and Ozawa 1995
; Ozawa 1995
; Nishino et al. 1996
; Ingman et al. 2000
; Shin et al. 2000
; Tawata et al. 2000
; Maca-Meyer et al. 2001
), RFLPs (Ballinger et al. 1992
; Torroni et al. 1993b,
1994
; Starikovskaya et al. 1998
; Schurr et al. 1999
; Derbeneva et al. 2002
), and HVS-I (and -II) sequences from Japan, Korea, central Asia, Southeast Asia, mainland China, and Taiwan (Horai and Hayasaka 1990
; Horai et al. 1996
; Kolman, Sambuughin, and Bermingham 1996
; Lee et al. 1997
; Comas et al. 1998
; Pfeiffer et al. 1998
; Seo et al. 1998
; Nishimaki et al. 1999
; Redd and Stoneking 1999
; Qian et al. 2001
), and have compared these data with a sample of 69 mtDNAs from southern China (Han Chinese), for which the two hypervariable segments (HVS-I, HVS-II) and specific coding region sites were analyzed. This allows us a better recognition of several limbs, which deeply branch off from the Eurasian mtDNA tree, as well as the identification of region-specific boughs and twigs that might testify to prehistoric settlement processes in the eastern fringe of Asia.
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Methods |
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Results |
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In the Asian-specific trunk M the combination of the currently available data (see fig. 2
) suggests that the limbs D, G, and M9 may all stem from a common node which is distinguished from the ancestral node of the M trunk solely by C at position 16362. The branching point, however, is somewhat ambiguous because position 16362 is highly variable (Hasegawa et al. 1993
) and the boughs of G differ at it. The limb M9 is defined by a transition at 4491 (as inferred from the data of Herrnstadt et al. 2002
) and thus carries the boughs E and M9a (previously referred to as M9 by Yao et al. 2002
). The next limb of M, called M7 here, is well supported by complete sequences: it is defined by transitions at 6455 and 9824, the latter of which is recognized by the gain of a HinfI site at 9820. The limb M7 branches further into three boughs, M7a, M7b, and M7c (see fig. 3
). The bough M7b was already identified by the loss of a HincII site at 7853 and distinguished as a group by Ballinger et al. (1992)
. M7c is not yet exactly characterized by coding region sites and is difficult to distinguish from other M subgroups on the basis of HVS-I alone. Another major limb, M8 (Yao et al. 2002
), is defined by transitions at 4715, 8584, 16298 and transversions at 7196 and 15487. Its principal boughs are the sister haplogroups C, Z, and a new haplogroup, M8a, that is characterized by transitions at 14470, 16184, and 16319 (Yao et al. 2002
). M also has a major limb, named Q by Forster et al. (2001)
, in Papua New Guinea as well as at least one limb in Australia.
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To clarify the positions of the East Asian haplogroups stemming from the pan-Eurasian trunk N, we also analyzed five West Asian mtDNAs belonging to haplogroups A, Y, W, and N1a (defined by transitions at 1719, 10238, 12501, 16172, and a transversion at 16147), and an unspecified offshoot of N. It turns out (see table 1
) that the East and West Asian limbs of N do not share any mutations, which implies an early split of the West Eurasian, South Asian (Kivisild et al. 1999a,
1999b
), and East Asian founder lineages. For haplogroup R we may anticipate a similar situation.
It should be emphasized that the abundant HVS-I information alone, without support from coding region sites, may be quite misleading in a number of cases. For instance, HVS-I sequences bearing the transition at 16295 may belong to either M7c or a novel M subgroup (characterized by transitions at 200, 215, 318, and 326 in HVS-II; see Yao et al. 2002
). The distinction of A4 and A5 from A* currently hinges upon a single hypervariable HVS-I site for each. More problematically, a HVS-I sequence differing from the Cambridge reference sequence (CRS) only at 16223 and 16362 (by transitions) can belong to any of the haplogroups D, E, G; the seeming R motif of transitions at 16245 and 16362 in fact characterizes a bough of D4 (cf. sequence MP1 in Ozawa et al. 1991
); the CRS (belonging to haplogroup H) may even match M and F sequences within HVS-I (see 33 and 37 in table 1 ). Comparing just short stretches of HVS-I sequences could therefore easily create the impression of specific European and East Asian mtDNA affinities, e.g., as asserted by figure 3 in Wang et al. (2000)
. Their Linxi data likely encompass several haplotypes from haplogroup B4, the ancestral type of which cannot be distinguished from CRS within the short HVS-I stretch sequenced. Any subdivision of mtDNA into clusters based on HVS-I sequences alone, as attempted by Horai et al. (1996)
, thus runs into serious problems. For instance, only 10 of the 18 clusters proposed by Horai et al. (1996)
turn out to be monophyletic (as long as back mutations would not cause trouble): their clusters C1, C6, C11, C14, C17, and C18 by and large correspond to B4, A, D5, M8, M7b2, and M7b1, respectively, whereas C1, C4, C7, and C15 constitute subclades of Y1, F1a, G2a, and M7a1, respectively. The potentially paraphyletic clusters C5, C8, C9, and C10 would essentially cover D4 but inevitably also include some other M haplotypes. The remaining four clusters (C2, C9, C12, and C16) constitute poly- or paraphyletic groups.
Although considerable differences in the geographic distribution of the Asian-specific haplogroups can already be revealed by comparing RFLP profiles of Siberian and Southeast Asian populations (Wallace 1995
), a finer resolution is obtained when extending the marker list on the mtDNA molecule. Haplogroups A, C, D, G, Y, and Z almost completely cover the mtDNA pool of Northeast Asians, whereas in Southeast Asians C, Y, or Z mtDNAs have rarely been found, but instead haplogroups B and F are predominant. N9a is, compared with its sister bough Y, widely spread, although at very low frequencies, among most East Asian populations considered here. Considering the geographic distribution of the boughs and twigs we see further regional patterns. In contrast to A4, which is widely spread, the A5 twig, with its low diversity suggesting shallow time depth, is specific to Koreans and Japanese (see fig. 4
). Similarly, B4 is the prevailing bough in haplogroup B (see fig. 2
), covering all haplogroup B types in Native Americans and Polynesians. B5 is found most frequent, accounting for about one third to one half of the B types, in eastern China, Korea, and Japan (Horai and Hayasaka 1990
; Horai et al. 1996
; Seo et al. 1998
; Nishimaki et al. 1999
). D4 seems to be the predominant bough of D (see fig. 2
), but as a whole it cannot be identified without coding region markers. D5 is characterized by a transition at 16189 in conjunction with the reversal of the RFLP marker for M (caused by a transition at 10397); it is most frequent in southern China but rare or absent in Central Asians and Siberians. E1 is so far found only in Southeast Asia (Ballinger et al. 1992
; our table 1
); what was called E in the Tibetan data (Torroni et al. 1994
) seems to be mixed with G2a (as signalized by 16227), and what was labeled E in the Asian mtDNA tree of Herrnstadt et al. (2002
, fig. 2
) turns out to constitute a mixed bag of M1, M7c, M9a, and real E haplotypes. F1a is the main branch of F (see fig. 2
) in Southeast Asia, whereas F1b is more frequent in Central Asians and Mongols, Koreans, and Japanese. F2, being much less frequent, may have a wide geographic distribution, as judged from the few occurrences of F2a. It seems that G1 is restricted to Northeast Siberia. G2a is highest among Central Asians (8.8%) and also above 3% in Tibetans and Ainu and rare or absent among southern Chinese, Vietnamese, island Southeast Asians (including Ryukyuans), and Siberians. G3 is not yet well screened, but evidently it is seen in Korea, Mongolia, and Central Asia. Y1 seems to be restricted to Northeast Asian populations and Ainu.
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In summary, we see characteristic regional features at several levels of the mtDNA phylogeny that testify to geographic structure (cf. Yao et al. 2002
). The tentative interpretation of this structuring is best accomplished when taking additional information about climatic conditions and archaeological findings into consideration, so that the genetic data can be used to address hypotheses about early or recent prehistoric events in East Asia.
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Discussion |
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In contrast to M7, the sharing of haplogroups A5, B5, C, F1a, N9a, and Z between Koreans and Japanese and their virtual absence in Ryukyuans and Ainu indicate later migrations and contacts between Korea and Japan. This is probably mainly due to the influx of Yayoi people (2,300 years ago) who brought agriculture and the Japanic language (Janhunen 1996
) to Japan. It is then remarkable in view of those events that the variation seen in M7 is not shuffled between Koreans and Japanese, quite in contrast to B4. This could point to the considerable geographic substructure of the Korean mtDNA pool at that time (paralleling the probable linguistic situation (Janhunen 1996
), so that the migrants carried only a limited number of M7 types (perhaps M7c1 types and the ancestral type of M7a together with a one-step descendant).
The presence of Y1 lineages among Ainu points to another migration route, namely, from the native Siberian populations to the northernmost populations of the Japanese islands. This mitochondrial connection fits well with the archaeological record (Imamura 1996
) and classical anthropological data (Hanihara 1998
). The peopling of Japan can therefore be seen as a complex process with the early pioneer settlement and several recent migrations which affected the resident populations differentially. By and large, the mtDNA findings support the opinions of Hanihara (1993)
and Kazumichi (1993)
.
The now emerging picture of the East Asian mtDNA tree that incorporates complete mtDNA information helps to shed light on prehistoric human migrations to and within the eastern belt of Asia. Quite consistent with the Y-chromosome data (Su et al. 1999
), mtDNA analyses show that although East Asian haplotypes are regionally specific, they all derive (together with the West Eurasian haplotypes) ultimately from one or two ancestral lineages of African origin. Subdividing the hierarchy of the mtDNA tree into limbs, boughs, and twigs is instrumental for telling apart the settlement processes of any particular region in appropriate time scale. We have demonstrated by way of example that the limbs and boughs, geographically widespread, reflect the earliest events in the settlement of East Asia, whereas the twigs of greater geographic specificity can be of value to uncover more recent events. The broad claim that in East Asia "there is ... almost no structure in the mtDNA differences among regions" and that "mtDNA phylogeny ... could not reveal much of interest about population history here" (Ding et al. 2000
) is clearly unjustified and rather reflects insufficient resolution of the used mtDNA markers and lack of phylogenetic reasoning.
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Acknowledgements |
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Footnotes |
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Abbreviations: RFLP, restriction fragment length polymorphism; CRS, Cambridge reference sequence; HVS-I (and -II), first (and second) hypervariable segment.
Keywords: human mitochondrial DNA
population genetics
phylogeography
Address for correspondence and reprints: Toomas Kivisild, Estonian Biocentre, Riia 23, Tartu 51010, Estonia. tkivisil{at}ebc.ee
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