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Y chromosomal DNA variation in east Asian populations and its potential for inferring the peopling of Korea.
Kim W, Shin DJ, Harihara S, Kim YJ.
Department of Biology, Dankook University, Cheonan, Choong-Nam, Republic of Korea. wookkim@ansco.dankook.ac.kr
We have examined variations of five polymorphic loci (DYS287, DXYS5Y, SRY465, DYS19, and DXYS156Y) on the Y chromosome in samples from a total of 1260 males in eight ethnic groups of East Asia. We found four unique haplotypes constructed from three biallelic markers in these samples of East Asians. The Japanese population was characterized by a relatively high frequency of either the haplotype I-2b (-/Y2/T) or II-1 (+/Y1/C). These dual patterns of the distribution of Y chromosomes (I-2b/II-1) were also found in Korea, although they were present at relatively low frequencies. The haplotype II-1 was present in Northeast Asian populations (Chinese, Japanese, Koreans, and Mongolians) only, except for one male from the Thai population among the Southeast Asian populations (Indonesians, Philippines, Thais, and Vietnamese). The Japanese were revealed to have the highest frequency of this haplotype (27.5%), followed by Koreans (2.9%), Mongolians (2.6%), and mainland Chinese (2.2%). In contrast, the frequency of the haplotype I-2b was found to be 17.1% in the Japanese, 9.5% in Indonesian, 6.3% in Korean, 3.8% in Vietnamese, and 2.7% in Thai samples. These findings suggested that the chromosomes of haplotype I-2b were likely derived from certain areas of Northeast Asia, the region closest to Southeast Asia. Phylogenetic analysis using the neighbor-joining tree also reflected a general distinction between Southeast and Northeast Asian populations. The phylogeny revealed a closer genetic relationship between Japanese and Koreans than to the other surveyed Asian populations. Based on the result of the dual patterns of the haplotype distribution, it is more likely that the population structure of Koreans may not have evolved from a single ancient population derived from Northeast Asians, but through dual infusions of Y chromosomes entering Korea from two different waves of East Asians.
PMID: 10721667 [PubMed - indexed for MEDLINE]

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
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.

Fig. 3 Principal components (PC) analysis of haplogroup frequencies in 11 east Asian populations (circle Koreans, open diamonds southeast populations, closed diamonds northeast populations)
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
http://www.journals.uchicago.edu/AJHG/jour...3/42338/42338.h tml
Y-Chromosome Evidence of Southern Origin of the East AsianSpecific Haplogroup O3-M122
Hong Shi,1,2,6 Yong-li Dong,3 Bo Wen,4 Chun-Jie Xiao,3 Peter A. Underhill,5 Pei-dong Shen,5 Ranajit Chakraborty,7 Li Jin,4,7 and Bing Su1,2,7
1Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology and 2Kunming Primate Research Center, Chinese Academy of Sciences, 3Key Laboratory of Bio-resources Conservation and Utilization and Human Genetics Center, Yunnan University, Kunming, China; 4State Key Laboratory of Genetic Engineering and Center for Anthropological Studies, School of Life Sciences, Fudan University, Shanghai; 5Department of Genetics, Stanford University, Stanford, CA; 6Graduate School of Chinese Academy of Science, Beijing; and 7Center for Genome Information, University of Cincinnati, Cincinnati
Received March 14, 2005; accepted for publication June 29, 2005; electronically published July 14, 2005.
The prehistoric peopling of East Asia by modern humans remains controversial with respect to early population migrations. Here, we present a systematic sampling and genetic screening of an East Asianspecific Y-chromosome haplogroup (O3-M122) in 2,332 individuals from diverse East Asian populations. Our results indicate that the O3-M122 lineage is dominant in East Asian populations, with an average frequency of 44.3%. The microsatellite data show that the O3-M122 haplotypes in southern East Asia are more diverse than those in northern East Asia, suggesting a southern origin of the O3-M122 mutation. It was estimated that the early northward migration of the O3-M122 lineages in East Asia occurred 25,00030,000 years ago, consistent with the fossil records of modern humans in East Asia.
It should be noted that when we discuss the origin and migration of human populations, a time periodwhich part of the human-population history is under scrutinyshould be clearly defined. Recent population movement and admixture could wipe out or significantly diminish the original genetic signatures of early population movements. Therefore, to extract information for modern human origin and early population movements that happened before the Neolithic period, population-specific markers, such as SNP markers on the Y chromosome, become useful for the study of regional population movements (Jobling and Tyler-Smith 2003). At the same time, recent gene flow between distantly related populations can also be identified and removed in an analysis based on population specificity. Hence, in this sense, extreme caution should be exercised in selection of genetic markers in the study of the origin and early migrations of a continental population, because genetic variations introduced through recent gene flow could create false interpretations, as in two previous studies (Ding et al. 2000; Karafet et al. 2001). The same logic also applies to the selection of populations; ethnic populations with long histories of inhabitation in a region are always preferred for inferring early population histories.
In East Asian populations, there are three regionally distributed (East Asianspecific) Y-chromosome haplogroups under the M175 lineage (fig. 1)O3-M122, O2-M95, and O1-M119together accounting for 57% of the Y chromosomes in East Asian populations (table 1). The O3-M122 has the highest frequency (41.8% on average) (fig. 2) in East Asians, especially in Han Chinese (52.06% in northern Han and 53.72% in southern Han) (table 1), and it is absent outside East Asia. Previous studies have shown that O2-M95 and O1-M119 are prevalent in SEAS and probably originated in the south (Su et al. 1999, 2000a; Wen et al. 2004a, 2004b) (table 1). Therefore, tracing the origin of O3-M122 became critical for a full understanding of the origin and early migrations of modern East Asians.

The frequency distribution of the O3-M122 haplotypes in East Asian and other continental populations. The data used were from published studies (Su et al. 1999, 2000a, 2000b; Qian et al. 2000; Semino et al. 2000; Underhill et al. 2000; Karafet et al. 2001; Lell et al. 2002; Jin et al. 2003; Wen et al. 2004a).

Fig. 2. Frequency distributions of the eight Y-chromosome haplotypes for the 14 global populations, with their approximate geographic locations. The frequencies of the eight haplotypes are shown as colored pie charts (for color codes, see upper left insert). JP Japanese
Only four Japanese populations exhibited ht1 (defined only by YAP+) at various frequencies (also see Table 1). The highest frequency (87.5%) was found in JP-Ainu, followed by JP-Okinawa (55.6%) living in the southwestern islands of Japan, JP-Honshu (36.6%), and JP-Kyushu (27.9%). The ht2 haplotype (defined by YAP+/M15+) was found in only two males, one each from Thais and Thai-Khmers; ht3 (defined by YAP+/SRY4064-A) was completely absent in the Asian populations examined, whereas Jewish in the Uzbekistan and African populations had this haplotype with a frequency of 28.3% and 100%, respectively. Thus, the YAP+ lineage was found in restricted populations among Asian populations, consistent with previous reports (Hammer and Horai 1995; Hammer et al. 1997; Shinka et al. 1999).
The ht4 haplotype (defined only by M9-G) was widely distributed among north, east, and southeast Asian populations, except for the Ainu. This haplotype was frequent (60.5%) in overall Asian populations (Table 1). Among them, the Han Chinese and southeast Asian populations were characterized by high frequencies ranging from 81.0% to 96.0%. In contrast to ht4, ht5 (defined by M9-G/DYS257108-A) and ht6 (defined by M9-G/DYS257108-A/SRY10831-A) were small contributors to Asian populations. The highest frequency of ht5 was observed in Nivkhi (19.0%) and that of the ht6 in Thai-Khmers (10.8%). The ht5 haplotype is widely distributed among European, Asian, and Native American populations and is proposed to be one of the candidates for founder haplotypes in the Americas (Karafet et al. 1999). Furthermore, high frequencies of ht6 were observed in north Europe, central Asia, and India (Karafet et al. 1999). Thus, the presence of ht5 in Nivkhi may account for the founder effect of peopling of the Americas.
The ht7 haplotype (defined by RPS4Y-T) was also widely distributed throughout Asia with the exceptions of Malaysia and the Philippines, whereas this was absent in two non-Asian populations. The highest frequency of ht7 was found in Buryats (83.6%), followed by Nivkhi (38.1%). Thus, the geographic distribution of ht7 in Asia appears to contrast with that of ht4.
Only eight individuals (1.4%) in Asia belonged to ht8, which was the major haplotype in Jewish population (Table 1). The ht8 haplotype may not be useful for inferring population relatedness among Asian populations because it is defined by no mutations. Additional Y-polymorphic markers such as M89 and M168 (Underhill et al. 2000; Ke et al. 2001) will be needed to investigate details of the formation of modern Asian populations.
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