Inland post-glacial dispersal in East Asia revealed by mitochondrial haplogroup M9a'b
- Min-Sheng Peng1, 2, 6,
- Malliya Gounder Palanichamy3,
- Yong-Gang Yao4,
- Bikash Mitra3, 5,
- Yao-Ting Cheng1, 2, 6,
- Mian Zhao1, 2, 6,
- Jia Liu3,
- Hua-Wei Wang3,
- Hui Pan1, 2, 6,
- Wen-Zhi Wang1, 2, 6,
- A-Mei Zhang4, 6,
- Wen Zhang4, 6,
- Dong Wang4, 6,
- Yang Zou4, 6,
- Yang Yang3,
- Tapas Kumar Chaudhuri5,
- Qing-Peng Kong1, 2Email author and
- Ya-Ping Zhang1, 2, 3Email author
© Peng et al; licensee BioMed Central Ltd. 2011
Received: 13 October 2010
Accepted: 10 January 2011
Published: 10 January 2011
Archaeological studies have revealed a series of cultural changes around the Last Glacial Maximum in East Asia; whether these changes left any signatures in the gene pool of East Asians remains poorly indicated. To achieve deeper insights into the demographic history of modern humans in East Asia around the Last Glacial Maximum, we extensively analyzed mitochondrial DNA haplogroup M9a'b, a specific haplogroup that was suggested to have some potential for tracing the migration around the Last Glacial Maximum in East Eurasia.
A total of 837 M9a'b mitochondrial DNAs (583 from the literature, while the remaining 254 were newly collected in this study) pinpointed from over 28,000 subjects residing across East Eurasia were studied here. Fifty-nine representative samples were further selected for total mitochondrial DNA sequencing so we could better understand the phylogeny within M9a'b. Based on the updated phylogeny, an extensive phylogeographic analysis was carried out to reveal the differentiation of haplogroup M9a'b and to reconstruct the dispersal histories.
Our results indicated that southern China and/or Southeast Asia likely served as the source of some post-Last Glacial Maximum dispersal(s). The detailed dissection of haplogroup M9a'b revealed the existence of an inland dispersal in mainland East Asia during the post-glacial period. It was this dispersal that expanded not only to western China but also to northeast India and the south Himalaya region. A similar phylogeographic distribution pattern was also observed for haplogroup F1c, thus substantiating our proposition. This inland post-glacial dispersal was in agreement with the spread of the Mesolithic culture originating in South China and northern Vietnam.
The climatic oscillation and the related ecological changes around the Last Glacial Maximum (LGM; approximately 26.5 to 19 kilo-years ago (kya))  were suggested to exert substantial influence on prehistoric migrations and demographic changes in modern humans . In East Asia, archaeological studies have indicated that great changes occurred in the wake of the LGM [3, 4]. For instance, the microblade technology appeared and became popular during the LGM in northern China ; some early settlements were abandoned  and people probably moved to the south due to the deteriorating environmental conditions . After the LGM, improved climate allowed humans to re-colonize the high latitude regions . However, whether the ancient dispersals around the LGM left any detectable genetic footprints in the gene pool of the contemporary East Asians was still elusive.
In the past decades, genetic data of mitochondrial DNA (mtDNA) and the non-recombining region of Y-chromosome (NRY) have been widely employed to reconstruct human prehistory [9, 10]. In Europe, the detailed phylogeographic dissection of matrilineal pools has discerned some haplogroups as the candidate markers for tracing the dispersal(s) after the LGM, which could be assigned as the Late Glacial (before the Holocene) and the post-glacial (after the Younger Dryas but before the Neolithic) re-colonization, respectively . Recently, this strategy has also been applied to other regions (for example, West Asia , South Asia , and Southeast Asia ), yielding many valuable insights into the prehistoric demographic events around the LGM.
To trace the ancient dispersal of modern humans in East Asia around the LGM, we carried out a detailed phylogeographic analysis on a high resolution mtDNA marker. We focused our attention particularly on East Eurasian specific mtDNA haplogroup M9a'b for four reasons: 1) M9a'b distributes widely in mainland East Asia  and is relatively concentrated in Tibet (approximately 19.2%) [15, 16] and its surrounding regions, including Nepal (approximately 11.6%) , Sikkim (approximately 11.7%)  and northeast India (approximately 8.6%) [18, 19]. 2) The phylogeny of haplogroup M9a'b indicated that this clade might be involved in some northward migrations into East Asia from Southeast Asia . 3) The coalescent time estimates of certain sub-haplogroups of M9a'b, for example, M9a (approximately 12 to 15 kya) [14, 16] and M9d (approximately 12 kya) , suggested that these lineages were likely associated with some post-LGM dispersal(s) in East Asia , especially in Tibet [15, 16]. 4) In addition to its high frequency, the relatively high genetic diversity, as revealed by the mtDNA control region hypervariable segment I (HVS-I) information in Tibet , suggested that Tibet might serve as the potential differentiation center of M9a'b sub-haplogroups. All these lines of evidence appeared to imply that Tibet might be a candidate source for the post-LGM dispersal in East Asia. Together, the detailed dissection of haplogroup M9a'b would provide insightful information for the ancient movement of modern humans in East Asia around the LGM.
M9a'b phylogenetic tree based on mtDNA genome information
Based on the updated M9a'b phylogeny, some interesting features could be discerned. With the exception of M9a1, most basal branches of M9a were distributed in southern China (6/15) and Southeast Asia (7/15); this pattern suggested that M9a might have a southern origin. The distribution pattern of M9a1 was rather complex: although this haplogroup did bear some genetic imprints of southern origin by harboring a basal lineage (that is, HN-H H27) from southern China, its effect had actually extended to northern China and Japan (for example, M9a1a1a, M9a1a1b, and M9a1a1c1a), as well as, western China (that is, southwestern China, northwestern China, and Tibet), northeast India (including Bangladesh), and the south Himalaya region (for example, M9a1b1, M9a1a2, and M9a1a1c1b). Based on this pattern, it seemed that haplogroup M9a1 had most likely been involved in some northward and westward dispersal(s) in East Asia.
Coalescence age estimates
Estimated coalescence ages of mtDNA haplogroup M9a'b and its sub-haplogroups based on different calibration rates.
Entire mitochondrial genome
Only synonymous mutations
Transitions in 16090 to 16365
M9a* (w/o M9a1)
M9a1b* (w/o M9a1b1)
M9a1a1* (w/o M9a1a1c)
M9a1a1c1* (w/o M9a1a1c1b)
Our phylogeographic analysis of haplogroup M9a'b further revealed some distinct distribution patterns of its sub-haplogroups. In particular, M9a1b and M9a1a2 showed a restricted distribution in western China, Myanmar, northeast India, and the south Himalaya region (Figure 4; see Additional file 2), but were virtually very rare or absent in northern China and Northeast Asia and even southern China (the suggested place of origin of M9a'b and M9a1), indicating that both haplogroups might have distinct origins from the other M9a'b sub-haplogroups. Meanwhile, M9a1a2 and M9a1b coincidentally shared a similar expansion age (approximately 9 to 12 kya; Table 1), which indicated that both haplogroups might have been involved in the same demographic event. Together, the current distribution pattern of haplogroups M9a1b and M9a1a2 was likely attributed to an inland post-glacial dispersal event, which started from southern China along with the differentiation of M9a1 (approximately 17 to 21 kya; Table 1; Figure 5b), then moved westward to western China, and finally to northeast India and the south Himalaya region (Figure 5c). Nevertheless, the phylogeographic pattern of M9a1a1 suggested some northward Late Glacial dispersal(s). In particular, the enrichment of haplogroup M9a1a1c1b in Tibet was likely to be explained by some recent local expansions, such as the Neolithic expansion [28, 29] in this region.
The proper interpretation of the obtained genetic data to reconstruct complex colonization scenarios would benefit from the incorporation of archaeological materials. After the LGM, around 12 to 15 kya, great cultural changes in South China and northern Vietnam were suggested to be associated with the prevalence of the Mesolithic culture, such as the Hoabinhian culture [27, 35] and the third stage of Bailiandong culture [26, 36]. The expansions of these Mesolithic cultures in southern China and Southeast Asia were already discussed in some recent studies [37, 38]. Intriguingly, the timing for our proposed inland post-glacial dispersal scenario was largely overlapped with the Mesolithic period, and more importantly, this inland route from southwestern China to northeast India and the south Himalaya region was in coincidence with the Hoabinhian links connecting southwestern China , northeast India , and Nepal [41, 42] (Figure 5c). It seemed that the advanced technology (for example, pottery [26, 36, 43]) and the improved climate would be the major factors in triggering the post-glacial dispersal. However, other factors such as the dispersal of language groups and the expansion of agriculture could not be neglected completely. Considering some major branches within M9a'b were relatively concentrated in different Tibeto-Burman and Khasi-Khmuic populations (see Additional file 1), the dispersals of Tibeto-Burman  and Austro-Asiatic populations , together with the intergroup genetic admixture , were likely to shape the current distribution pattern of M9a'b. Further work on more genetic markers (for example, NRY, genome-wide single nucleotide polymorphisms, and even ancient DNA) with extensive sampling will be required to further confirm our speculation regarding the prehistoric peopling scenario(s) in East Asia.
Our comprehensive phylogeographic analyses of mtDNA haplogroup M9a'b revealed that southern China and/or Southeast Asia served as a source of the post-LGM dispersal in East Asia. Most importantly, our results provided the first direct genetic evidence in support of the existence of an inland dispersal in mainland East Asia from southern China, through western China, to northeast India and the south Himalaya region. This dispersal was likely triggered by the improved climate and the advanced Mesolithic culture, and had played important roles in shaping the matrilineal gene pool of modern East Asians.
A total of 837 candidate M9a'b mtDNA samples (583 from the literature and 254 from this study; see Additional file 1), with specific mtDNA control region motif 16223-16234-16362-153 and/or coding region diagnostic site 3394 or 4491, were pinpointed from over 28,000 subjects residing across East Eurasia (Figure 1; see Additional file 2). All subjects recruited in this study were interviewed with informed consent to ascertain their ethnic affiliations. To better understand the phylogeny within M9a'b, besides the 61 published M9a'b mtDNA genome sequences that were retrieved from the literature and GenBank (see Additional file 4), an additional 59 representatives were selected from our own samples for complete mtDNA sequencing, with a special attempt to cover the widest range of internal variation within the haplogroup . By virtue of the updated phylogeny of haplogroup M9a'b, we further classified the remaining M9a'b candidates based on the specific coding region motifs (for our own samples; see Additional file 1) and/or by matching and near-matching [32, 47] with the well-defined M9a'b lineages (for the reported mtDNAs from the literature). Using this strategy, the vast majority of the M9a'b mtDNA samples (771/837) could be unambiguously allocated into specific sub-haplogroups within M9a'b, whereas the remaining 66 sequences (all from the literature) could only be roughly assigned into M9a'b* due to lack of further information (see Additional file 1).
The sequencing protocol and phylogeny reconstruction were performed as fully described before [48, 49], and some caveats for data quality-control were followed during the data generation and handling [50, 51]. Sequences were edited and aligned by using Lasergene (DNAStar Inc., Madison, Wisconsin, USA) and variations were scored relative to the revised Cambridge Reference Sequence (rCRS) . For the C-stretch length variants in the control region, we followed the rules proposed by Bandelt and Parson . The transition at 16519 and the C-length polymorphisms in regions 16180 to 16193 and 303 to 315 were disregarded in the analyses. The classification of the variants of each mtDNA genomes was performed with mtDNA GeneSyn 1.0 http://www.ipatimup.pt/downloads/mtDNAGeneSyn.zip and MitoTool http://mitotool.org/index.html. Sequences generated in this study have been deposited in GenBank (Accession Nos. GQ337542, GQ337575, GQ337588, and HM346881 to HM346936).
Phylogenetic tree construction and data analysis
The phylogenetic tree of 120 M9a'b complete mtDNA sequences was reconstructed manually and checked by NETWORK 4.516 http://www.fluxus-engineering.com/sharenet.htm. For the HVS data and/or partial coding region, the median-joining network of 837 M9a'b mtDNA sequences was constructed manually and was further checked by using the Network 4.516 . The counter maps of spatial frequencies  were constructed to elaborate the geographic distribution patterns of haplogroup M9a'b and its sub-haplogroups using the Kriging algorithm of Surfer 8.0 (Golden Software Inc. Golden, Colorado, USA).
The average sequence divergence (ρ) of the haplotypes to their most recent common ancestor, accompanied by a heuristic estimate of the standard error (σ), was calculated as fully described before [58, 59]. Then, the ρ ± σ value was converted into the coalescent age for certain haplogroup by using the most recently proposed calibration rates for mtDNA mutations  and only synonymous substitutions , respectively. For the control region, we adopted the rate of 18,845 years per transition between 16090 and 16365 .
Last Glacial Maximum
non-recombining region of Y-chromosome
revised Cambridge Reference Sequence.
We thank all participants involved in this study. We also thank Chun-Ling Zhu, Shi-Fang Wu, Jun-Dong He, Shi-Kang Gou, Feng Gao, Nguyen Ngoc Sang, and Ji-Shan Wang for their technical assistance. We thank Dr. Mannis van Oven for the discussion about the nomenclature of mtDNA haplogroups. This study was supported by grants from the National Natural Science Foundation of China (30621092 and 30900797), and the Bureau of Science and Technology of Yunnan Province (2009CI119).
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