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Thread: The Dual Origins of the Koreans

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    Post Koreans

    Human Genetics

    © Springer-Verlag 2003
    10.1007/s00439-003-1019-0

    Original Investigation
    Y-chromosomal DNA haplogroups and their implications for the dual origins of the Koreans
    Han-Jun Jin1, Kyoung-Don Kwak1, Michael F. Hammer2, Yutaka Nakahori3, Toshikatsu Shinka3, Ju-Won Lee3, Feng Jin4, Xuming Jia4, Chris Tyler-Smith5 and Wook Kim1

    (1) Department of Biological Sciences, Dankook University, 330-714 Cheonan, Korea
    (2) Laboratory of Molecular Systematics and Evolution, University of Arizona, Tucson, AZ 85721, USA
    (3) Department of Public Health, School of Medicine, University of Tokushima, 770-0085 Tokushima, Japan
    (4) Institute of Genetics, Chinese Academy of Sciences, Beijing, China
    (5) Department of Biochemistry, University of Oxford, Oxford, OX1 3QU, UK


    Wook Kim
    Email: wookkim@dankook.ac.kr
    Phone: +82-41-5503441
    Fax: +82-41-5503441

    Received: 18 April 2003 Accepted: 31 July 2003 Published online: 18 September 2003

    Abstract We have analyzed eight Y-chromosomal binary markers (YAP, RPS4Y711, M9, M175, LINE1, SRY+465, 47z, and M95) and three Y-STR markers (DYS390, DYS391, and DYS393) in 738 males from 11 ethnic groups in east Asia in order to study the male lineage history of Korea. Haplogroup DE-YAP was found at a high frequency only in Japan but was also present at low frequencies in northeast Asia, including 2.5% in Korea, suggesting a northern origin for these chromosomes. Haplogroup C-RPS4Y711 was present in Korea and Manchuria at moderate frequencies: higher than in populations from southeast Asia, but lower than those in the northeast, which may imply a northern Asian expansion of these lineages, perhaps from Mongolia or Siberia. The major Y-chromosomal expansions in east Asia were those of haplogroup O-M175 (and its sublineages). This haplogroup is likely to have originated in southern east Asia and subsequently expanded to all of east Asia. The moderate frequency of one sublineage in the Koreans, haplogroup O-LINE1 (12.5%), could be a result of interaction with Chinese populations. The age of another sublineage, haplogroup O-SRY+465, and Y-STR haplotype diversity provide evidence for relatively recent male migration, originally from China, through Korea into Japan. In conclusion, the distribution pattern of Y-chromosomal haplogroups reveals the complex origin of the Koreans, resulting from genetic contributions involving the northern Asian settlement and range expansions mostly from southern-to-northern China.

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    Introduction
    Studies of the early peopling of east Asia have long been a subject of interest in the field of human evolutionary history. Current hypotheses can be classified into two major models of the early migration routes into east Asia. The first model postulates that a southeast Asian origin is most likely, followed by a northward migration (Turner 1990). Recent genetic surveys with autosomal microsatellite markers (Chu et al. 1998) and Y-chromosomal binary markers (Su et al. 1999) support this model. In contrast, the second model suggests a bi- and/or multidirectional route: one migration through central Asia and one through southeast Asia (Nei and Roychoudhury 1993; Cavalli-Sforza et al. 1994; Karafet et al. 2001). Ding et al. (2000) have also noted that southeast Asia is not the homeland for northeast Asian populations, but the potential importance of more recent gene flow from central Asia needs to be stressed for the peopling of northeast Asia. Since Korea and Japan lie between the southeast and northeast Asian gene pools, their population genetic data can give us valuable information about the prehistoric migration route(s) and population expansions in east Asia.

    The Koreans are generally considered a northeast Asian group, since the Korean peninsula is bounded to the north by China, to the northeast by Russia, and to the south by the Korean Strait and Japan. The Korean Peninsula and Japanese Archipelago were contiguous land before the rise in sea levels between 10,000 and 7,000 years ago (Glover 1980). Based on the results of archeological data, the earliest modern human lithic cultures are found from 25,000 to 45,000 years ago in the Altai Mountains and southeastern Siberia and the Korean Peninsula (Vasil'ev 1993; Choi 1993). Anthropological and/or archeological evidence suggests that the early Korean population was related to Mongolian ethnic groups who inhabited the general area of the Altai Mountains in central Asia (Kim 1970). Therefore, the ancient Koreans (proto-Koreans) may have shared a common origin with the northeast Asian groups who inhabited the general area of the Altai Mountains and Lake Baikal regions of southeastern Siberia.

    There is also evidence for recent migration and range expansions via north China to Korea (Chard 1974; Hammer and Horai 1995; Yun 1998; Choi and Rhee 2001). According to Korea's founding myths, the Ancient Chosun (the first state-level society) was established around 2,333 BC in the region of southern Manchuria but later moved into the Pyongyang area of northwest Korea. Recent northeastward migration from China, beginning in the 3rd century BC, led to the decline of the Ancient Chosun, with various Ancient States in the regions of southern Manchuria and the Korean Peninsula emerging. In addition, archeological evidence implies that rice cultivation had spread to all parts of the Korean Peninsula by around 1,000 BC, introduced from the Yangtze River basin in southern China (Choi and Rhee 2001).

    Studies of classical genetic markers (protein and nuclear DNA) show that Koreans tend to have a close genetic affinity with Mongolians among northeast Asians (Goedde et al. 1987; Saha and Tay 1992; Hong et al. 1993). In contrast, genetic surveys of mitochondrial DNA (mtDNA) variation indicate that the Koreans are more closely related to the Chinese and Japanese among east Asian populations (Harihara et al. 1988; Horai et al. 1996; Jin et al. 1999). Recent studies of Y-chromosomal DNA markers show that the Koreans possess lineages from both northeast and southeast Asia (Kim et al. 2000; Kwak and Kim 2001; Karafet et al. 2001). These results have led us to consider that the peopling of Korea is likely to have involved multiple events, and that different aspects could be revealed by different molecular genetic markers and DNA samples. Thus, further markers and DNAs from diverse regions of east Asia are required to explore the origin and genetic history of modern Koreans.

    The present study, therefore, was designed to trace the male lineage history of the Koreans and their relationships to other east Asian ethnic groups. We analyzed eight Y-chromosomal binary markers (YAP, RPS4Y711, M9, M175, LINE1, SRY+465, 47z, and M95) and three Y-STR markers (DYS390, DYS391, and DYS393) in samples from a total of 738 males from several regions of southeast and northeast Asia. We report that the peopling of Korea can be seen as a complex process with genetic contributions involving the northern Asian settlement and range expansions mostly from southern-to-northern China. A recent migration event leading to a Y-chromosome contribution from Korea to Japan is also discussed.


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    Materials and methods
    DNA samples
    We analyzed a total of 738 male DNA samples, collected from 11 east Asian populations, as shown in Table 1. The DNA samples included subsets of the samples examined by Kim et al. (2000), although the exact number of subjects for each population occasionally varies between these studies. In addition, we included the following new Chinese and Mongolian samples: 39 Yunnan Han, 44 Manchurians, and 49 Khalkhs. DNA was prepared from whole blood by the standard method (Sambrook et al. 1989) or was extracted from buccal cells according to the procedure of Richards et al. (1993).
    Table 1 Allele frequencies of eight Y-chromosomal binary markers in east Asian populations
    No. (%) of

    RPS4Y711
    YAP
    M9
    M175
    LINE1
    SRY+465
    47z
    M95

    Population (n)
    C
    T
    +

    C
    G
    +

    +

    C
    T
    Y1
    Y2
    C
    T

    Northeast Asians:

    N. Chinese (113)

    Beijing-Han (69)
    65 (94.2)
    4 (5.8)
    1 (1.4)
    68 (98.6)
    17 (24.6)
    52 (75.4)
    20 (29.0)
    49 (71.0)
    10 (14.5)
    59 (85.5)
    65 (94.2)
    4 (5.8)
    69 (100.0)
    0
    69 (100.0)
    0

    Manchurians (44)
    34 (77.3)
    10 (22.7)
    1 (2.3)
    43 (97.7)
    11 25.0)
    33 (75.0)
    13 (29.5)
    31 (70.5)
    2 (4.5)
    42 (95.5)
    37 (84.1)
    7 (15.9)
    39 (88.6)
    5 (11.4)
    44 (100.0)
    0

    Japanese (108)
    98 (90.7)
    10 (9.3)
    37 (34.3)
    71 (65.7)
    47 (43.5)
    61 (56.5)
    49 (45.4)
    59 (54.6)
    2 (1.9)
    106 (98.1)
    80 (74.1)
    28 (25.9)
    87 (80.6)
    21 (19.4)
    107 (99.1)
    1 (0.9)

    Koreans (160)
    136 (85.0)
    24 (15.0)
    4 (2.5)
    156 (97.5)
    29 (18.1)
    131 (81.9)
    41 (25.6)
    119 (74.4)
    20 (12.5)
    140 (87.5)
    129 (80.6)
    31 (19.4)
    151 (94.4)
    9 (5.6)
    160 (100.0)
    0

    Mongolians (100)

    Buryats (51)
    32 (62.7)
    19 (37.3)
    2 (3.9)
    49 (96.1)
    23 (45.1)
    28 (54.9)
    40 (78.4)
    11 (21.6)
    3 (5.9)
    48 (94.1)
    50 (98.0)
    1 (2.0)
    51 (100.0)
    0
    51 (100.0)
    0

    Khalkhs (49)
    28 (57.1)
    21 (42.9)
    1 (2.0)
    48 (98.0)
    24 (49.0)
    25 (51.0)
    36 (73.5)
    13 (26.5)
    3 (6.1)
    46 (93.9)
    49 (100.0)
    0
    49 (100.0)
    0
    49 (100.0)
    0

    Southeast Asians:

    S. Chinese (39)

    Yunnan (39)
    36 (92.3)
    3 (7.7)
    1 (2.6)
    38 (97.4)
    5 (12.8)
    34 (87.2)
    14 (35.9)
    25 (64.1)
    5 (12.8)
    34 (87.2)
    39 (100.0)
    0
    39 (100.0)
    0
    38 (97.4)
    1 (2.6)

    Indonesians (36)
    33 (91.7)
    3 (8.3)
    0
    36 (100.0)
    3 (8.3)
    33 (91.7)
    5 (13.9)
    31 (86.1)
    4 (11.1)
    32 (88.9)
    29 (80.6)
    7 (19.4)
    35 (97.2)
    1 (2.8)
    26 (72.2)
    10 (27.8)

    Philippines (77)
    74 (96.1)
    3 (3.9)
    0
    77 (100.0)
    6 (7.8)
    71 (92.2)
    14 (18.2)
    63 (81.8)
    9 (11.7)
    68 (88.3)
    76 (98.7)
    1 (1.3)
    77 (100.0)
    0
    76 (98.7)
    1 (1.3)

    Thais (55)
    55 (100.0)
    0
    1 (1.8)
    54 (98.2)
    5 (9.1)
    50 (90.9)
    8 (14.5)
    47 (85.5)
    3 (5.5)
    52 (94.5)
    52 (94.5)
    3 (5.5)
    53 (96.4)
    2 (3.6)
    29 (52.7)
    26 (47.3)

    Vietnamese (50)
    39 (78.0)
    11 (22.0)
    0
    50 (100.0)
    11 (22.0)
    39 (78.0)
    13 (26.0)
    37 (74.0)
    2 (4.0)
    48 (96.0)
    43 (86.0)
    7 (14.0)
    48 (96.0)
    2 (4.0)
    45 (90.0)
    5 (10.0)


    Genotyping of DNA polymorphisms and nomenclature
    Eight Y-chromosomal binary markers were genotyped in all individuals sampled. They included YAP (Hammer 1994), RPS4Y711 (Bergen et al. 1999), M9 (Underhill et al. 1997), M175 (Underhill et al. 2001), LINE1 (Santos et al. 2000), SRY+465 (Shinka et al. 1999), 47z (Nakagome et al. 1992), and M95 (Su et al. 1999), known to be polymorphic in east Asia. The YAP Alu insertion was analyzed by using the primer set and conditions reported by Hammer and Horai (1995). The RPS4Y711 (C to T substitution), M9 (C to G substitution), M175 (-5 bp), and M95 (C to T substitution) markers were amplified by using the following primer sets and modifications reported by Bergen et al. (1999) and Underhill et al. (1997, 2001): RPS4Y711, 5'-TATCTCCTCTTCTATTGCAG-3' and 5'-CCACAAGGGGGAAAAAACAC-3'; M9, 5'-GCAGCATATAAAACTTTCAG-3' and 5'-CTCAAGCGTAAATGTACTGT-3'; M175, 5'-TTGAGCAAGAAAAATAGTACCCA-3' and 5'-CTCCATTCTTAACTATCTCAGGGA-3'; M95, 5'-GAGTGGAAATCAAGATGCCAAG-3' and 5'-GACTCTCCTAAGCCTACAGG-3'; each polymerase chain reaction (PCR) was performed in a total volume of 25 l containing 25 ng genomic DNA, 10 pM each primer, 0.2 mM dNTPs, 2.0 mM MgCl2, 50 mM KCl, 10 mM TRIS-HCl (pH 8.3), and 1.5 U AmpliTaq DNA polymerase (Perkin-Elmer). The PCR cycling conditions for the RPS4Y711 marker used a first denaturation step at 94°C for 5 min, and then 35 cycles at 94°C for 45 s, 50°C for 45 s, 72°C for 1 min, and a final extension at 72°C for 3 min. The cycling conditions for M9 were 94°C for 5 min, and then 35 cycles at 94°C for 45 s, 42°C for 45 s, 72°C for 1 min, and a final extension at 72°C for 3 min. M175 was amplified under PCR conditions of 95°C for 10 min, and then 35 cycles at 94°C for 45 s, 55°C for 45 s, 72°C for 1 min, and a final extension at 72°C for 10 min. The cycling conditions for the M95 marker were 94°C for 5 min, and then 35 cycles at 94°C for 1 min, 60°C for 1 min, 72°C for 1.5 min, and a final extension at 72°C for 3 min. The PCR products for RPS4Y711 and M9 were digested with BslI and HinfI enzymes, respectively, and fractionated on 2% agarose gels. For typing M175, the PCR products were separated by electrophoresis on a 6% denaturing polyacrylamide gel (PAGE) containing 8 M Urea, in 1×TBE buffer (0.09 M TRIS-borate, 0.002 M EDTA, pH 8.3), for 3.5 h at a constant 50 W, with a separation distance of 40 cm. Bands were visualized by silver staining as described elsewhere (Rabilloud et al. 1988). After PCR amplification, the C to T transition mutation of the M95 marker was detected by the PCR/single-strand conformation polymorphism method described by Kutach et al. (1999). The band patterns of their alleles were evaluated on a 10% native PAGE gel in a 10°C cold chamber and visualized by silver staining. The LINE1 insertion was scored as described by Santos et al. (2000). An allele-specific PCR amplification method was performed to genotype SRY+465 (C to T substitution), as described by Kim et al. (2000). The allelic variation of 47z was analyzed by using the PCR/restriction fragment length polymorphism method reported by Shin et al. (1998): only the PCR product amplified from the Y2 allele has a recognition sequence for the restriction enzyme StuI.

    We also examined three Y-chromosomal short tandem repeat (STR) loci (DYS390, DYS391, and DYS393) in almost all samples. The allelic variations at these STR loci were determined by multiplex PCR amplification (Shin et al. 2001) and followed the allele nomenclature of Kayser et al. (1997).

    For binary markers, we followed the terminology and nomenclature proposed by the Y Chromosome Consortium (2002). The terms "haplogroup" and "haplotype" are used according to de Knijff (2000): "haplogroup" refers to lineages from the non-recombining portion of the Y-chromosome (NRY) defined by binary polymorphisms alone, and "haplotype" is reserved for all sublineages of haplogroups that are defined by variation at STRs on the NRY.

    Data analyses
    Principal components analysis of haplogroup frequencies in population samples was carried out by using SPSS 11.0. Coalescence times for subsets of chromosomes defined by the binary markers were estimated by using BATWING (Wilson and Balding 1998), assuming a generation time of 30 years. Locus-specific STR mutation rates based on the measurements of Kayser et al. (2000) were used, and various demographic models were tested in different runs of the program. The mean haplotype diversity of three Y-STR loci in different populations was estimated by the method of Nei (1987).


    --------------------------------------------------------------------------------

    Results and discussion
    We observed nine different Y haplogroups by using the eight binary markers (Fig. 1). The structure of this tree is consistent with previous results from east Asia (Su at al. 1999; Karafet et al. 2001; Tajima et al. 2002; Kayser et al. 2003). The frequency distributions of the eight binary markers and corresponding haplogroups are listed in Tables 1 and 2 and displayed in Fig. 2. The east Asian populations were characterized by a high frequency (96.6%) of three major Y-chromosomal lineages (haplogroups DE-YAP, C-RPS4Y711, and K-M9). These three distinct lineages coalesce to the M168-T lineage, which probably originated in Africa (Underhill et al. 2000; Ke et al. 2001). Our results, therefore, provide additional data confirming that the east Asian Y-chromosomal gene pool is almost completely contained within these three Y lineages (Tajima et al. 2002).

    Fig. 1 Y-chromosome parsimonious tree showing the evolutionary relationship of nine haplogroups constructed from the eight binary markers. Nomenclature is according to the Y Chromosome Consortium (2002)

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    Table 2 Distribution of Y-chromosomal haplogroup frequencies in east Asian populations
    Population (n)
    No. (%) of

    Y*(xC,DE,K)
    C-RPS4Y711
    DE-YAP
    K*-M9
    O*-M175
    O-LINE1
    O-SRY+465
    O-47z
    O-M95

    Northeast Asians:

    N. Chinese (113)

    Beijing-Han (69)
    12 (17.4)
    4 (5.8)
    1 (1.4)
    3 (4.3)
    35 (50.7)
    10 (14.5)
    4 (5.8)
    0
    0

    Manchurian (44)
    0
    10 (22.7)
    1 (2.3)
    2 (4.5)
    22 (50.0)
    2 (4.5)
    2 (4.5)
    5 (11.4)
    0

    Japanese (108)
    0
    10 (9.3)
    37 (34.3)
    2 (1.9)
    28 (25.9)
    2 (1.9)
    7 (6.5)
    21 (19.4)
    1 (0.9)

    Koreans (160)
    1 (0.6)
    24 (15.0)
    4 (2.5)
    12 (7.5)
    68 (42.5)
    20 (12.5)
    22 (13.8)
    9 (5.6)
    0

    Mongolians (100)

    Buryats (51)
    2 (3.9)
    19 (37.3)
    2 (3.9)
    17 (33.3)
    7 (13.7)
    3 (5.9)
    1 (2.0)
    0
    0

    Khalkhs (49)
    2 (4.1)
    21 (42.9)
    1 (2.0)
    12 (24.5)
    10 (20.4)
    3 (6.1)
    0
    0
    0

    Southeast Asians:

    S. Chinese (39)

    Yunnan (39)
    1(2.6)
    3 (7.7)
    1 (2.6)
    9 (23.1)
    19 (48.7)
    5 (12.8)
    0
    0
    1 (2.6)

    Indonesians (36)
    0
    3 (8.3)
    0
    2 (5.6)
    10 (27.8)
    4 (11.1)
    6 (16.7)
    1 (2.8)
    10 (27.8)

    Philippines (77)
    3 (3.9)
    3 (3.9)
    0
    8 (10.4)
    52 (67.5)
    9 (11.7)
    1 (1.3)
    0
    1 (1.3)

    Thais (55)
    4 (7.3)
    0
    1 (1.8)
    3 (5.5)
    15 (27.3)
    3 (5.5)
    1 (1.8)
    2 (3.6)
    26 (47.3)

    Vietnamese (50)
    0
    11 (22.0)
    0
    2 (4.0)
    23 (46.0)
    2 (4.0)
    5 (10.0)
    2 (4.0)
    5 (10.0)



    Fig. 2 Distribution of Y haplogroups in east Asia. Circle area is proportional to sample size, and the nine haplogroups are represented by different colors

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    The distribution of Y-chromosomal variation surveyed here reveals significant genetic differences among east Asian populations. Haplogroup DE-YAP (the YAP+ allele) was present at high frequency only in the Japanese and was rare in other parts of east Asia (Table 2, Fig. 2). This result is consistent with previous findings of YAP+ chromosomes only in populations from Japan and Tibet in east Asia (Hammer and Horai 1995; Hammer et al. 1997; Kim et al. 2000; Tajima at al. 2002). However, haplogroup DE-YAP is also found at low frequencies in all the other northeast Asian populations sampled here (2.4% overall, excluding the Japanese; 9.6%, including the Japanese), but only in two of the southern populations (0.8% overall), suggesting that the Korean YAP+ chromosomes are unlikely to have been derived from a southeast Asian source. The prevalence of the YAP+ allele in central Asian populations suggests a genetic contribution to the east Asian populations from the northwest, probably from central Asia (Altheide and Hammer 1997; Jin and Su 2000; Karafet et al. 2001).

    Haplogroups C-RPS4Y711 and K-M9 were widely but not evenly distributed in the east Asian populations. Haplogroup C-RPS4Y711 appears to be the predominant northeast Asian haplogroup, with high frequencies in Mongolians (Buryats, 37.3%; Khalkhs, 42.9%) and Manchurians (22.7%; Table 2, Fig. 2). The moderate frequency of haplogroup C-RPS4Y711 Y-chromosomes in Korea (15.0%) implies a genetic influence from northern populations of east Asia, starting possibly in east Siberia. Su and Jin (2001) suggest that the RPS4Y711-T chromosome originated in east Asia, probably in the southeast, and then expanded to the north (Siberia), based on the genetic diversity of Y-STR markers. However, the observed low Y-STR diversity of haplogroup C-RPS4Y711 chromosomes in their surveys of Siberian and central Asian populations compared with east Asian populations could also be explained by a more northern (Mongolian and/or Siberian) origin followed by genetic drift resulting from small effective population sizes (Pakendorf et al. 2002). Recently, Cavalli-Sforza and Feldman (2003) have suggested that haplogroup C-RPS4Y711 expanded both through a southern route from Africa (e.g., India) to Oceania, and a northern one to Mongolia, Siberia, and eventually to northwest America. Further genetic surveys are required to test these hypotheses, with additional markers and more samples from diverse regions of Asia.

    In contrast, M9-G Y-chromosomes show an opposing distribution to those carrying RPS4Y711-T in east Asia: they are more frequent in southern populations than in northern ones, showing a clinal variation from about 90% to 60% (Table 1). The haplogroups carrying the M9-G mutation and additional sublineages of M9-G in Korea appear to be at an intermediate frequency (81.9%) between southeast and northeast Asian populations. This result implies that the Korean population may be influenced by both the northeast and southeast Asian populations. Even within haplogroup O, the most frequent Korean STR haplotype (23-10-13 with the markers DYS390-DYS391-DYS393, 19% of haplogroup O; Table 3) is the most frequent in the Philippines (27%), whereas the second most frequent Korean haplotype (24-10-12, 16%) is the most frequent in Manchuria (45%). Thus, the distribution of haplogroups K-M9 and C-RPS4Y711 may reflect dispersals from both north and south. The settlement of each region at different times needs to be considered in order to understand the peopling of east Asia. Recently, Karafet et al. (2001) have noted that realistic explanations for the peopling of east Asia have to accommodate more complex multidirectional biological and cultural influences than earlier models have allowed.
    Table 3 Haplotype distribution and diversity of three Y-STR markers in chromosomes carrying the M175–5bp deletion (ah haplotype diversity)
    Y-STR Haplotype (390-391-393)
    No. in (%)

    Manchurian (n=31)
    Beijing-Han (n=49)
    Koreans (n=119)
    Philippines (n=63)
    Thais (n=47)

    20-10-16
    0
    0
    1 (0.8)
    0
    0

    21-9-12
    0
    0
    0
    1 (1.6)
    0

    21-9-14
    0
    0
    0
    1 (1.6)
    0

    21-10-14
    0
    0
    0
    1 (1.6)
    0

    22-9-13
    0
    0
    0
    0
    1 (2.1)

    22-9-14
    0
    0
    0
    0
    1 (2.1)

    22-10-12
    0
    3 (6.1)
    3 (2.5)
    0
    0

    22-10-13
    1 (3.2)
    1 (2.0)
    9 (7.6)
    2 (3.2)
    1 (2.1)

    22-10-14
    0
    0
    1 (0.8)
    0
    1 (2.1)

    22-11-12
    0
    0
    1 (0.8)
    0
    0

    22-11-13
    0
    0
    2 (1.7)
    0
    0

    22-11-14
    0
    0
    1 (0.8)
    0
    0

    23-9-12
    0
    0
    3 (2.5)
    0
    0

    23-9-13
    0
    0
    1 (0.8)
    0
    0

    23-10-12
    3 (9.7)
    9 (18.4)
    17 (14.3)
    5 (7.9)
    1 (2.1)

    23-10-13
    2 (6.5)
    4 (8.2)
    23 (19.3)
    17 (27.0)
    3 (6.4)

    23-10-15
    0
    1 (2.0)
    0
    0
    0

    23-11-12
    0
    3 (6.1)
    8 (6.7)
    0
    0

    23-11-13
    0
    5 (10.2)
    8 (6.7)
    3 (4.8)
    0

    23-11-14
    0
    0
    0
    0
    1 (2.1)

    23-11-15
    0
    0
    1 (0.8)
    0
    0

    24-9-12
    0
    0
    1 (0.8)
    0
    0

    24-9-13
    0
    0
    1 (0.8)
    0
    0

    24-10-11
    0
    0
    1 (0.8)
    0
    0

    24-10-12
    14 (45.1)
    8 (16.3)
    19 (16.0)
    3 (4.8)
    5 (10.6)

    24-10-13
    3 (9.7)
    4 (8.2)
    1 (0.8)
    11 (17.5)
    2 (4.2)

    24-10-14
    3 (9.7)
    2 (4.1)
    1 (0.8)
    1 (1.6)
    2 (4.2)

    24-10-15
    0
    0
    0
    0
    1 (2.1)

    24-11-12
    0
    1 (2.0)
    3 (2.5)
    2 (3.2)
    0

    24-11-13
    0
    0
    3 (2.5)
    2 (3.2)
    1 (2.1)

    24-11-14
    0
    1 (2.0)
    0
    0
    11 (23.4)

    25-9-12
    1 (3.2)
    0
    0
    0
    0

    25-10-11
    0
    0
    1 (0.8)
    0
    0

    25-10-12
    4 (12.9)
    1 (2.0)
    7 (5.9)
    2 (3.2)
    0

    25-10-13
    0
    1 (2.0)
    0
    8 (12.7)
    1 (2.1)

    25-10-14
    0
    0
    0
    0
    4 (8.5)

    25-10-15
    0
    0
    0
    0
    2 (4.2)

    25-11-12
    0
    1 (2.0)
    1 (0.8)
    2 (3.2)
    1 (2.1)

    25-11-13
    0
    2 (4.1)
    1 (0.8)
    1 (1.6)
    0

    25-11-14
    0
    1 (2.0)
    0
    0
    6 (12.8)

    25-11-15
    0
    0
    0
    0
    1 (2.1)

    26-10-12
    0
    1 (2.0)
    0
    0
    0

    26-10-14
    0
    0
    0
    0
    1 (2.1)

    26-11-15
    0
    0
    0
    1 (1.6)
    0

    ah
    0.770
    0.920
    0.902
    0.877
    0.915


    As shown in Table 1, most east Asian populations share a common genetic feature of high frequencies of M175-derived chromosomes (>70%), which form a sublineage of haplogroup K-M9. Based on the distribution of Y haplogroups and Y-STR haplotype diversity, which is slightly higher in the southern populations than the northern (0.90 vs 0.86 on average; Table 3), the major expansions in east Asia carried haplogroup O-M175 (and its sublineages) and may have originated in southern east Asia, before expanding into all of east Asia. When employing BATWING, the obtained coalescence time depended on the demographic model used, but when both a period of constant size and an expansion were allowed, 8,100 (3,500–18,900) years was obtained (Table 4). Given the uncertainty, these results are concordant with previous reports of a northward migration of modern humans into eastern Asia during the last Ice Age (75,000–15,000 years ago; Su et al. 1999, 2000).
    Table 4 BATWING estimates of coalescence times (in years) of the chromosomes carrying the M175 mutation, or the subset carrying the SRY+465 mutation, based on the diversity at three Y-STRs
    Demographic model
    M175
    SRY+465

    Constant size
    10,700 (5,300–24,920)
    3,300 (1,600–7,100)

    Constant then expanding
    8,100 (3,500–18,900)
    2,800 (1,100–5,700)

    Always expanding
    3,300 (2,200–5,500)
    2,000 (1,200–3,400)


    Although haplogroup O-LINE1 was found at moderate to low frequencies in all the east Asian populations examined (8.5% overall), Han Chinese have the highest frequency of this L1 retroposon insertion polymorphism (15%). We therefore suspect that this lineage might have emerged in China (probably southern China) and been carried south and east, eventually extending into the surrounding regions. This result is consistent with recent surveys showing that O-LINE1 Y-chromosomes are present at high frequencies in samples of the Han Chinese and two minority populations, the Tujia and Miao from Hunan located in the southern areas of the Yangtze River (Santos et al. 2000; Kwak and Kim 2001). The moderate frequency of haplogroup O-LINE1 Y-chromosomes in the Korean population (12.5%) may have resulted from its interaction with Chinese populations. Southeast Asian populations, except for the Philippines, are characterized by a high frequency of haplogroup O-M95 (16.7%; Table 2, Fig. 2). This result is concordant with recent surveys carried out by Su et al. (1999) and Kayser et al. (2003). Based on the result of the O-M95 Y-chromosome distribution, Koreans are not closely related to the most southern east Asians but tend to be more related to the population of southern-to-northern China.

    The prevalence of haplogroups carrying the SRY+465-T allele in Korean and Japanese populations suggests a strong genetic affinity between these two populations (Tables 1 and 2, Fig. 2). Haplogroup O-47z Y-chromosomes are direct descendants (a sublineage) of haplogroup O-SRY+465 (Fig. 1). Shinka et al. (1999) reported that Y-chromosomes carrying the SRY+465-T allele were not present in most European and African males examined in their survey. Lin et al. (1994) suggested that the O-47z Y-chromosomes (Y2 allele) might have originated from an ancestral population in Henan or southern parts of Shanxi near the Yellow River in China. Many ancient Chinese moved from the estuary of the Yellow River to the middle and downstream regions of the Yangtze River ~4,000 years ago (Ruofu and Yip 1993; Su et al. 2000). With increasing political chaos in the Chinese mainland during its Warring Period (476–221 BC), many Chinese moved further southward and eastward, and eventually inhabited all of China (Eberhard 1980). There is also historical evidence that many Chinese fled and sought refuge in the Korean Ancient Chosun during the Warring Period (Yun 1998; Choi and Rhee 2001). In addition, archeological evidence indicates that rice cultivation had spread to all parts of the Korean peninsula around 1,000 BC, introduced from the Yangtze River basin in southern China (Choi and Rhee 2001). The recent range expansion and introduction of rice cultivation from southern China may have resulted in the appearance of Y-chromosomal lineages carrying haplogroup O-M175-derived markers in Korea.

    Recent surveys have also inferred that a large infusion of haplogroup O-47z Y-chromosomes entered Japan with the Yayoi migration from the Korean peninsula starting 2,300 years ago (Hammer and Horai 1995; Altheide and Hammer 1997). Since the Y-chromosome lineage carrying the SRY+465-T mutation is a direct ancestor to haplogroup O-47z (Fig. 1), we analyzed Y-STR variation in those individuals with the SRY+465-T mutation (59 Korean and Japanese individuals; Table 5). The coalescence time was again dependent on the demographic model, but assuming a constant size followed by expansion, a time of 2,800 (1,100–5,700) years was obtained, consistent with its spread at the time of the Yayoi migration. The Y-STR haplotype diversity in those individuals with the SRY+465-T mutation in Korea (0.832) is much higher than that of Japan (0.609; Table 5). Therefore, these results provide convincing evidence for recent male migration, originally from China, into Japan moving through Korea.
    Table 5 Haplotype distribution and diversity of three Y-STR markers linked with the SRY+465-T mutation (ah haplotype diversity)
    Y-STR Haplotype (390-391-393)
    No. in (%)

    Korea (n=31)
    Japan (n=28)

    22-10-12
    1 (3.2)
    0

    22-10-13
    9 (29.0)
    17 (60.7)

    22-10-14
    1 (3.2)
    2 (7.1)

    22-11-12
    1 (3.2)
    0

    22-11-13
    1 (3.2)
    2 (7.1)

    23-9-12
    1 (3.2)
    0

    23-10-12
    2 (6.5)
    0

    23-10-13
    9 (29.0)
    5 (17.9)

    23-11-13
    5 (16.1)
    1 (3.6)

    24-9-12
    0
    1 (3.6)

    24-9-13
    1 (3.2)
    0

    ah
    0.832
    0.609


    In this study, the Koreans appear to be most closely related overall to the Manchurians among east Asian ethnic groups (Fig. 2), although a principal components analysis of haplogroup frequencies reveals that they also cluster with populations from Yunnan and Vietnam (Fig. 3). The genetic relationship with Manchuria is consistent with the historical evidence that the Ancient Chosun, the first state-level society, was established in the region of southern Manchuria and later moved into the Pyongyang area of the northwestern Korean Peninsula. Based on archeological and anthropological data, the early Korean population possibly had a common origin in the northern regions of the Altai Mountains and Lake Baikal of southeastern Siberia (Han 1995; Choi and Rhee 2001). Recent studies of mtDNA (Kivisild et al. 2002) and the Y-chromosome (Karafet et al. 2001) have also indicated that Koreans possess lineages from both the southern and the northern haplogroup complex. In conclusion, the peopling of Korea can be seen as a complex process with an initial northern Asian settlement followed by several migrations, mostly from southern-to-northern China.

    Fig. 3 Principal components (PC) analysis of haplogroup frequencies in 11 east Asian populations (circle Koreans, open diamonds southeast populations, closed diamonds northeast populations)

    --------------------------------------------------------------------------------

    Acknowledgements We thank L. Roewer for providing reference Y-STR DNA samples, P. Underhill for SNP genotyping information, and D.J. Shin for his helpful laboratory assistance and DNA sampling. We especially thank T. Karafet for useful comments on the manuscript. This work was supported by a grant from the Korean Science and Engineering Foundation (KOSEF F01-2001-000-20024-0).


    --------------------------------------------------------------------------------

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    Post The Dual Origins of the Koreans

    Y-chromosomal DNA haplogroups and their implications for the dual origins of the Koreans
    Han-Jun Jin1, Kyoung-Don Kwak1, Michael F. Hammer2, Yutaka Nakahori3, Toshikatsu Shinka3, Ju-Won Lee3, Feng Jin4, Xuming Jia4, Chris Tyler-Smith5 and Wook Kim1

    (1) Department of Biological Sciences, Dankook University, 330-714 Cheonan, Korea
    (2) Laboratory of Molecular Systematics and Evolution, University of Arizona, Tucson, AZ 85721, USA
    (3) Department of Public Health, School of Medicine, University of Tokushima, 770-0085 Tokushima, Japan
    (4) Institute of Genetics, Chinese Academy of Sciences, Beijing, China
    (5) Department of Biochemistry, University of Oxford, Oxford, OX1 3QU, UK

    Received: 18 April 2003 Accepted: 31 July 2003 Published online: 18 September 2003

    Abstract We have analyzed eight Y-chromosomal binary markers (YAP, RPS4Y711, M9, M175, LINE1, SRY+465, 47z, and M95) and three Y-STR markers (DYS390, DYS391, and DYS393) in 738 males from 11 ethnic groups in east Asia in order to study the male lineage history of Korea. Haplogroup DE-YAP was found at a high frequency only in Japan but was also present at low frequencies in northeast Asia, including 2.5% in Korea, suggesting a northern origin for these chromosomes. Haplogroup C-RPS4Y711 was present in Korea and Manchuria at moderate frequencies: higher than in populations from southeast Asia, but lower than those in the northeast, which may imply a northern Asian expansion of these lineages, perhaps from Mongolia or Siberia. The major Y-chromosomal expansions in east Asia were those of haplogroup O-M175 (and its sublineages). This haplogroup is likely to have originated in southern east Asia and subsequently expanded to all of east Asia. The moderate frequency of one sublineage in the Koreans, haplogroup O-LINE1 (12.5%), could be a result of interaction with Chinese populations. The age of another sublineage, haplogroup O-SRY+465, and Y-STR haplotype diversity provide evidence for relatively recent male migration, originally from China, through Korea into Japan. In conclusion, the distribution pattern of Y-chromosomal haplogroups reveals the complex origin of the Koreans, resulting from genetic contributions involving the northern Asian settlement and range expansions mostly from southern-to-northern China.

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    Smile Re: the dual origins of the Koreans

    Euclides, keep up the great work in posting this very helpful research!

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