* State Key Laboratory of Genetic Engineering and Center for Anthropological Studies, School of Life Sciences, Fudan University, Shanghai, China; Department of Biology and Human Genetics Center, Yunnan University, Kunming, China;
Guanxi University of Nationalities, Nanning, China;
Center for Genome Information, Department of Environmental Health, University of Cincinnati, Ohio
Correspondence: E-mail: lijin{at}fudan.edu.cn; li.jin{at}uc.edu.
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Abstract |
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Key Words: East Asia Hmong-Mien Genetic structure mtDNA haplogroup
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Introduction |
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Hmong-Mien is one of the major language families spoken in southern China and Southeast Asia. It contains 32 languages, and their speakers exceed 12 million in China alone (2000 Census). Archeological and historical studies have shown that protoH-M populations were associated with the Neolithic cultures that were found in the Middle Reach of the Yangtze River, i.e., Daxi Culture (5,3006,400 years before present [YBP]) and Qujialing Culture (4,6005,000 YBP), and the San-Miao tribes in Central-southern China (Fei 1999). However, no systematic genetic study has been reported to reveal the genetic structure and prehistory of the H-M populations.
Genetic differentiation between the southern and northern East Asian populations has been observed with classic markers (Cavalli-Sforza, Menozzi, and Piazza 1994; Xiao et al. 2000), mitochondrial DNA (mtDNA) (Yao et al. 2002a; Kivisild et al. 2002), and Y chromosome variations (Su et al. 1999; Jin and Su 2000; Karafet et al. 2001), although the mechanism that led to such differences remains controversial (Su et al. 1999; Ding et al. 2000; Jin and Su 2000; Karafet et al. 2001). The final revelation of the mechanism of the north-south division in East Asian peoples warrants an extensive accumulation of genetic data from East Asian populations, particularly from the understudied groups, such as the H-M-speaking populations.
Haploid and maternally inherited mtDNA is one of the most powerful tools in reconstructing the evolutionary history of human populations (Wallace, Brown, and Lott 1999; Cavalli-Sforza and Feldman 2003). The major structure of the phylogeny of mtDNA haplotypes found in East Asia is becoming increasingly robust, owing to the effort of combining the variations in the control and coding regions (Wallace, Brown, and Lott 1999; Yao et al. 2002a; Kivisild et al. 2002) and availability of increasing numbers of complete mtDNA sequences (Kong et al. 2003a). Specifically, macro-haplogroup M and N encompass almost all mtDNA lineages in East Asia. M encompasses the lineages of haplogroup D, G, M7, M8 (ancestral to the haplogroup C and Z), M9 etc., whereas N is composed of the lineages of A, B, R9 (ancestral to haplogroup F), and N9. By studying the distribution of these haplogroups and their sub-haplogroups, one can trace the migration of populations in East Asia, as exemplified by a recent account of peopling of Japan and Korea (Kivisild et al. 2002).
In this report, we present the results of a study of mtDNA diversity of the variations in the hypervariable segment 1 (HVS1) region, along with 16 diagnostic variants in the coding regions, in 537 individuals sampled from 17 H-M-speaking populations across East Asia. This is the first systematic study of the genetic structure of the H-M populations, aimed to investigate the matrilineal ancestry of the H-M populations and to provide more data for evaluating the genetic structure of East Asians. The understanding of the distribution of mtDNA variations also bears importance in the studies of mtDNA-associated diseases (Wallace, Brown, and Lott 1999).
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Material and Methods |
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Data Analysis
The 360-bp-long HVS1 sequences (1602416383) were edited and aligned against the revised Cambridge Reference Sequence (CRS; Andrews et al. 1999) using DNASTAR software (DNASTAR, Inc.). For quality control, we rechecked all the polymorphic sites in the chromatogram using DNSTAR software. And then, in comparison with the established phylogeny (Kivisild et al. 2002), the data set was checked using NETWORK software (www.fluxus-engineering.com) to test for potential errors (Bandelt et al. 2001). Overall, 537 HVS1 sequences from 17 H-M populations have been submitted to GenBank (Accession numbers AY546723AY547259).
Haplotype diversity (H) and nucleotide diversity () were used to evaluate the extent of within-population variation (Nei 1987). Probability of identity (Nei 1987) and FST were calculated to investigate between-population diversity. The genetic structure of populations was investigated by the analysis-of-molecular-variance approach (AMOVA; Excoffier, Smouse, and Quattro 1992). The calculations of diversity indices, FST and AMOVA were conducted on ARLEQUIN software (Schneider et al. 2000). An unrooted Neighbor-Joining tree was constructed by FST distances using MEGA 2.1 software (Kumar et al. 2001). The data sets of other East Asian populations4 A-A (Yao and Zhang 2002; L.J., unpublished data), 6 Altai (Yao et al. 2002b; Kong et al. 2003b), 10 Daic (Yao et al. 2002b; L.J., unpublished data), 10 northern Han, 15 southern Han (Oota et al. 2002; Yao et al. 2002a; Wen et al. 2004b), and 17 T-B populations (Yao et al. 2002b; Wen et al. 2004a)were integrated in these analyses. Correlation of genetic and geographic distance was tested by Mantel test, using ARLEQUIN software. Significance of correlation coefficient (r) was obtained by comparing with distribution of 1,000 random permutations.
Haplogroup affiliation of each mtDNA sequence was inferred based on the HVS1 motif and diagnostic variants in the coding regions, following Kivisild et al. (2002) and Kong et al. (2003a). Median joining networks (Bandelt, Forster, and Rohl 1999) were constructed by NETWORK software to investigate detailed relationships of the lineages within each haplogroup and to infer possible new haplogroups wherever applicable. The nomenclature of newly established (sub)-haplogroups followed Kong et al. (2003a). Coalescence time and its standard error of the haplogroups were calculated by the methods developed by Forster et al. (1996) and Saillard et al. (2000), respectively. To show genetic relationships between H-M and other East Asian populations, principal component analysis (PCA) was conducted by haplogroup frequencies, using SPSS10.0 software [SPSS Inc., Chicago, Ill.]). To avoid bias from estimating of haplogroup frequencies based on HVS1 sequences alone (Kivisild et al. 2002), in the PCA analysis, we used only the data sets typed in both the HVS1 and the coding regions (Yao et al. 2002a; 2003; Kivisild et al. 2002; Kong et al. 2003b; Wen et al. 2004a, 2004b; this study; L.J., unpublished data).
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Results |
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Of the 537 mtDNAs found in H-M, 9.5% (42 M*, 1 N*, and 11 R*) cannot be assigned to the presently defined haplogroups. Three M* mtDNAs share the HVS1 haplotype 16111162231623516362, a motif that is also found in two Zhuang samples (Yao et al. 2002b). The motif 161921622316292, an analog of west Euroasian haplogroup W, is observed in four M* samples, but it has not been seen in other East Asia populations. Ten Miao M* samples share the motif 1609316223163111636216381. This haplotype is very rare in other populations except for Naxi (Wen et al. 2004a), where its frequency is considerable (9%). Four R* mtDNAs carry both the 1618916311 motif and 10394 DdeI+. More effort is required to characterize these haplotypes.
Distribution of Haplogroups in the H-M Populations
Based on the phylogeny of East Asian mtDNA lineages (Kivisild et al. 2002; Kong et al. 2003a; this study), we inferred haplogroup affiliation for every mtDNA in this study, by considering both HVS1 and coding region variations. The haplotype frequencies in the H-M populations are presented in table 4. Some 43% of H-M mtDNAs belong to haplogroup M and its derived haplogroups (M7, M8, M8a, C, Z, D, and G); and the macro-haplogroup N and its nested lineages (A, B, F, R9, R, N9a, Y) account for 57% H-M mtDNAs.
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In the macro-haplogroup N, B and R9 (including F, R9b, and R9c) are the predominant lineages, with very high frequencies (30.2% for B and 19.8% for R9). Frequency of haplogroup B in the H-M populations is the highest in mainland East Asians (Yao, Watkins, and Zhang 2000). All the H-M populations carry haplogroup B mtDNAs, with its frequency ranging from 17% (in YMB) to 60% (in YDB). The B4 (18.2%) and B5 (11.7%) haplogroups encompass almost all haplogroup B mtDNAs in H-M, and B4a (9.3%) and B5a (11%) account for one third of B mtDNAs. B5a is very homogeneous in H-M: 42 of 59 B5a mtDNAs share the motif 161401618916266A, and the MJ network of B5a indicates a typical star-like phylogeny, whose coalescence time is estimated at 6,000 ± 2, 000 YBP. B4a itself contains many branches, which need to be further investigated. Over one third (38%, i.e., 19/50) of B4a mtDNAs in H-M bear the motif 16129161891621716261, which is rare in the other East Asian populations (only seen in 2 Shandong Han, 1 Yunnan Han, 1 Dai, and 1 Thai). Thus the time estimation of the age this lineage may contribute to understanding the peopling of the H-M populations. The time estimation for this lineage is 3,560 ± 2,050 YBP. The motif 16189162171626116357 is completely absent in other populations, and thus it turns out to be a H-Mspecific lineage. It was found in 7 H-M mtDNAs, and the time estimation is 26,000 ± 16,000 YBP. It should be noted that this estimate is somewhat imprecise because of the small sample size. B4e is another H-Mspecific lineage, which was found in 10 H-M mtDNAs and almost absent in the other populations (seen only in 1 Dai and 1 Vietnamese). Its age is 13,500 ± 9,500 YBP. Other haplogroup B lineages, B4b1, B4f, B5b, and B5b are distributed sporadically, with low frequencies in H-M.
Haplogroup F was observed in all the H-M populations (15.5% in total), and it appears to be the most frequent haplogroup in R9. More than half (54%) of F mtDNAs belong to the F1a lineage, which is the predominant F type in H-M and other southern East Asians (Kivisild et al. 2002). F1a1 and F1a1a account for one-third of F1a samples respectively. The estimated ages for H-M F1a1 and F1a1a are 18,000 ± 10,400 YBP and 8,600 ± 6,100 YBP, respectively. R9c, a newly defined haplogroup in this study, is observed only in 4 H-M samples. This rare haplogroup is found only in southern China and Southeast Asia. By including an additional 11 R9c samples (Oota et al. 2002; Yao et al. 2002a; Tajima et al. 2003; B.W, unpublished data), the age of R9c is estimated as 29,600 ± 16,300 YBP, appearing to be a deep lineage distributed in southern East Asia. Other R9 lineages, F1b, F1c, F2a, and F3 are seen in some populations with low frequencies.
N9 (including N9a and Y) and A are the other two haplogroups under the N branch. Haplogroup A was observed in 3% (16 of 537) of H-M mtDNAs, 56% (9/16) of which are concentrated in MHN. Frequency of haplogroup A in MHN is very high (8.7%), which is close to the frequency in northern populations. In contrast, it is absent or occurs as singletons in the other H-M populations. Haplogroup A6, which was observed in the Northern Han, Japanese, and Korean populations, occurs in some H-M populations as singletons. N9 consists of Y and N9a. Only one sample in the MHN belongs to Y, and N9a occurs in some populations with low frequency.
Population Cluster as Revealed by PCA
Figure 2 presents the PCA results conducted in H-M and other East Asian populations. Northern East Asians (NEA) and southern East Asians (SEA) are clearly separated by PC2 (accounting for 12.2% of the total variation), and the H-M populations fall entirely into the southern group. The H-M populations clustered together with other SEA groups (Daic, A-A, Southern Han [S. Han], and Southern Tibeto-Burman [STB]), indicating a general resemblance of the maternal lineages between H-Ms and other SEAs. Some H-Ms (MHN, MYN, YKM, YLO, YYM, YGS, and YMI) are closer to S. Han and STB, whereas the rest clustered with Daic and Austro-Asiatic groups, two typical SEA groups. Interestingly, Miao-Hunan (MHN) is closer to NEAs than other H-M populations. Its PC2 value (0.10) is higher than all the other H-Ms (PC2, mean 0.31, range 0.01, 0.64), although the difference is only marginally significant (t-test, P = 0.061). To explore possible influence of the difference of sample size on the PC results, we (1) removed those populations whose sample size was <20 in the PC analysis; (2) resampled 30 individuals from MHN (n = 103) and conducted PCA 20 times. These gave almost the same PCA results, indicating sample size has little influence on the PCA.
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Discussion |
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Archeologists and historians have suggested that the proto-H-M might be linked with the Neolithic culture in the Middle Reach of the Yangtze River in southern China (Fei 1999), including the Daxi Culture (5,3006,400 YBP) and the Qujialing Culture (4,6005,000 YBP). Haplogroup B5a, which is very homogeneous and shows a star-like phylogeny, accounts for 11% of H-M mtDNAs and exists in most of the H-M populations. The estimated age of B5a in H-M is 6,000 ± 2, 000 YBP. Another lineage, the motif 16129161891621716261, is strongly H-Mspecific and is present in 8 of the 17 H-M populations. The estimated age of this lineage is 3,560 ± 2, 050 YBP. Furthermore, 23 D4 mtDNAs from 10 H-M populations share the same motif ,190921622316362, which is very rare in other populations. Coalescence time of the D4 mtDNAs with this motif is estimated at 4,000 ± 2, 000 YBP. All these estimations are well in line with the age of the two aforementioned cultures excavated in southern China. The study of ancient DNA from the Daxi Culture and Qujialing Culture would be of great importance to verify the possible affiliations of H-M and these Neolithic cultures.
We have demonstrated that most H-M maternal lineages are of southern origin. The genetic relationship among H-Ms and other SEAs is another important issue that needs to be investigated. The results of average FST and AMOVA clearly indicated that H-M is closer to Daic and S. Han than to STB and A-A. Their geographic distributions could offer a reasonable explanation. Daic and S. Han are mainly distributed in Central-southern China, which was also populated by H-Ms, according to historical records. In contrast, A-As and STBs were mainly distributed in Southwestern China, an area to which H-Ms moved just during the past several hundreds years (Cang 1997). The Mantel test further demonstrated that the genetic and geographic distances correlate significantly, reflecting the influence of IBD, that is, that gene flows between H-Ms and their adjacent SEA populations had shaped their maternal genetic landscape to some extent.
The Miao populations are relatively distant from the Yao populations, as revealed by FST analysis and population tree analysis, as well as by the relatively lower frequencies of southern lineages (44.7% for MHN and 51.3% for MYN). In particular, MHN carries the highest frequency of the northern lineages with or without including haplogroup D (47% including D, 27% not including D). The proportion of northern lineages in MHN is significantly higher than that in other H-Ms (t-test, P = 0.017). This observation may be biased because the sample size of MHN (103) is much larger than the sample sizes of other H-Ms (average 27). We investigated the influence of the difference of sample sizes by resampling 30 individuals from HMN data 500 times. The resampling showed very similar proportions of NEA mtDNAs in MHN (average 0.464; 95% CI, 0.4550.472) to the real data (0.467), demonstrating no marked influence of sample size on our observation. Again, comparison of genetic distances, the population cluster based on the phylogenetic tree, and the PCA plot demonstrate a closer affinity of MHN for NEAs.
A famous legend concerning the ancient San-Miao tribe, thought to be the ancestor of present-day H-M populations, is of great interest. The San-Miao tribe expanded northward to the Yellow River drainage area; then, led by the Chiyou, they battled against the Yan-Huang tribe (one of the primary Sino-Tibetan ancestors) in Zhulu (in present-day Hubei Province near Beijing). The Chiyou were defeated and pushed back to the south before the Yan-Huang dominated the northern China. Our mtDNA data might provide some clues for tracing this march. As we showed earlier, the southern lineages account for only about 50% of Miao mtDNAs; most of the lineages prevalent in NEA are found in Miao-Hunan (MHN), which has the highest frequency of such haplogroups in the H-M populations. A careful inspection of the distribution of the northern mtDNA lineages revealed more information. A6 is almost absent in other southern populations, but it is present in Miao-Hunan. C5 is the dominating haplogroup C type in the southern populations; however, almost all haplogroup C mtDNAs are non-C5 in the two Miao populations. G3 is a very rare in NEA, and it is completely absent in the south. Surprisingly, two Miao-Hunan mtDNAs carry this haplogroup. These observations suggest that the Miao (Hmong) people may have more contact with the NEA.
In summary, we demonstrated that southern lineages account for the majority of the H-M mtDNA gene pool, a finding consistent with the southern origins of the H-M populations. The higher ratio of northern lineages observed in the Miao people suggests that they had more contacts with the northern East Asians. Our systematic study of H-M mtDNA diversity provides genetic evidence for the origin and migration of the H-M populations and the data for further investigation of the genetic structure of East Asians.
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Supplemental Material |
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Acknowledgements |
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Footnotes |
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