Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Genetic insights into the origins of Tibeto-Burman populations in the Himalayas

Abstract

The Himalayan mountain range has played a dual role in shaping the genetic landscape of the region by (1) delineating east–west migrations including the Silk Road and (2) restricting human dispersals, especially from the Indian subcontinent into the Tibetan plateau. In this study, 15 hypervariable autosomal STR loci were employed to evaluate the genetic relationships of three populations from Nepal (Kathmandu, Newar and Tamang) and a general collection from Tibet. These Himalayan groups were compared to geographically targeted worldwide populations as well as Tibeto-Burman (TB) speaking groups from Northeast India. Our results suggest a Northeast Asian origin for the Himalayan populations with subsequent gene flow from South Asia into the Kathmandu valley and the Newar population, corroborating a previous Y-chromosome study. In contrast, Tamang and Tibet exhibit limited genetic contributions from South Asia, possibly due to the orographic obstacle presented by the Himalayan massif. The TB groups from Northeast India are genetically distinct compared to their counterparts from the Himalayas probably resulting from prolonged isolation and/or founder effects.

Introduction

The Himalayan mountain range encompasses an unparalleled landscape featuring some of the planet's highest peaks providing a formidable barrier separating the Tibetan plateau from the Indian subcontinent.1 The region also constitutes an ethnic and linguistic contact zone as it marks a crossroad of three different religions (Islam, Hinduism and Buddhism) and two language families (Indo-European and Sino-Tibetan), with Sino-Tibetan partitioning into the Chinese and Tibeto-Burman (TB) subfamilies. Speakers of the latter represent the majority of the Himalayan inhabitants whereas the Indo-Europeans are restricted to the south of the cordillera.

The geo-political partitioning of TB-speaking groups include Tibet, Nepal, Northeast India, Bhutan, Burma and parts of Southeast Asia.2 Two opposing views on the origin of TB populations have been proposed. Both models invoke demic diffusion for the dispersal of the language subfamily. Su et al.3, 4 postulate the upper and middle Yellow River basin as the ancestral source of TB people. In contrast, van Driem5, 6 argues for the Yangtse River in Sichuan province as the homeland of TB speakers, with subsequent northward migrations to the fertile plains of the Yellow River valley where Neolithic civilizations flourished.

Our recent study on Y-chromosomal diversity in the Himalayan populations of Nepal and Tibet revealed high frequencies of East Asian-specific haplogroup O3a5-M134, congruent with earlier reports on TB groups,4, 7, 8, 9 suggesting a common ancestry for this language subfamily.1 This investigation also revealed elevated levels of South Asian-derived Y-haplogroup R1a1-M198 in the Nepalese populations of Kathmandu and Newar, indicating significant genetic influences from the Indian subcontinent, whereas the Himalayas served as a barrier to gene flow from the south into the Tibetan plateau.1 These findings are consistent with a recent mtDNA study,10 which reported reciprocal maternal gene flow between India and Nepal.

On the other hand, previous Y-chromosome studies characterizing the Tibetan people4, 11, 12 argue for Central Asian genetic contributions to account for the presence of Asian-specific YAP (Y Alu polymorphism) chromosomes (D-M174) in the plateau. Haplogroup D-M174 lineages are found at appreciable frequencies in the Andaman Islands of the Indian Ocean13 but only minimally in all East Asian populations with the exception of Japan.1, 4, 11, 12, 14, 15 Distinctive D-M174 subclades are observed in the Andaman Islands (D-M174*) and Japan (D2-M55), whereas Tibetans exhibit haplogroups D1-M15 and D3-P47.

In addition to the demic diffusion scenarios portrayed by linguistic and genetic studies,4, 5, 6 Aldenderfer and Yinong16 have proposed an acculturation mechanism to explain the spread of Neolithic civilizations throughout northwestern Tibet. The authors deem it unlikely that agricultural migrants from relatively low elevations in the eastern plateau acclimated to the alpine and desert steppes of the Changtang (northwestern Tibet) considering the physiological stresses imposed by the high altitudes. As a result, they find it more plausible for cultural and not migration to be the mechanism leading to the nomadic pastoralism currently practiced in the region.

Northeast Indian populations have been extensively studied due to their strategic location as well as their socio-cultural and linguistic diversity.9, 17, 18, 19, 20, 21, 22 This region, bordered by the Himalayas to the north and the Bay of Bengal in the south, connects the Indian subcontinent to East Asia. In a recent autosomal microsatellite study, the genetic affinities present among TB groups from Northeast India21 have been ascribed to geographic contiguity rather than linguistic affiliation. The same group suggested that, given its geographical proximity, Burma most likely provided the source population for the Manipur and Tripura territories, whereas those from the northern region (Arunachal Pradesh, Mizoram and Sikkim) have been populated primarily by Tibetans.21 Unfortunately, the study did not incorporate both probable parental source populations to assess their phylogenetic relationships to the Northeast Indian groups. Other studies based on Bhutanese and Nepalese Y-STR profiles revealed isolation and drift among these Himalayan collections, with a pronounced effect of drift observed in Bhutan. Nevertheless, haplotype sharing indicates possible gene flow between them or from a common source population.23, 24

Autosomal STRs are selectively neutral, hypervariable markers that vary solely on the basis of mutation and drift.25 They are distributed throughout the genome and biparentally inherited, as opposed to the uniparental Y-chromosome and mtDNA polymorphisms, providing a more holistic representation of the evolutionary and migratory events that have shaped modern populations. These attributes endow them with the high resolution necessary to assess phylogenetic relationships among closely related human groups.26, 27, 28, 29

Although several studies related to the Tibetan population utilizing autosomal markers have been previously published,30, 31, 32, 33, 34, 35 the current project is the first of its kind to perform comprehensive phylogenetic analyses in a statistically significant sample size. A set of 15 autosomal STR loci was employed to characterize three populations from Nepal (Newar, Tamang and Kathmandu) as well as the general populace from Tibet. These collections were compared to previously published geographically and ethnically targeted groups from East Asia, South Asia and Southwest Asia in an attempt to establish genetic relationships among them.

This study aims to provide information on the genetic origins of Tibetan and Nepalese populations. Our results suggest that these Himalayan populations are of Northeast Asian ancestry and that the Kathmandu and Newari collections have been significantly influenced by subsequent gene flow from South Asia. However, the genetic contribution of this latter region to the Tamang and Tibet is negligible, probably due to the physical barrier presented by the Himalayan massif. It is noteworthy that the three Nepalese populations (Kathmandu, Newar and Tamang) display strong genetic differentiation despite sharing close geographic confines, underscoring the need for studies of anthropologically well-defined ethnic groups. A second objective is to assess the phylogenetic relationships between our Himalayan populations and Northeast Indian TB peoples. Contrary to previously published Y-chromosome data,9 our work indicates that Northeast Indians are genetically distinct from the Himalayan and East Asian collections, a disparity that may be attributable to male founder effects.

Materials and methods

Sample collection and DNA isolation

Blood samples were collected with informed consent from 341 unrelated individuals from Tibet (153) and three populations from Nepal (188), namely Tamang (45), Newar (66) and Kathmandu (77). The ancestry of every person was recorded for a minimum of two generations. With the exception of the people of Kathmandu, who speak an Indo-European language (Nepali), members of the three other collections are TB speakers. The geographic locations of the populations are shown in Figure 1. Sample collections were performed in accordance with the ethical guidelines put forth by the institutions involved in this study. DNA was extracted by the standard phenol–chloroform and ethanol precipitation method as described in Antunez de Mayolo et al.36 and stored at −80 °C.

Figure 1
figure 1

Geographic locations of the Himalayan and reference populations examined in this study.

DNA amplification and STR genotyping

DNA samples were amplified at 15 autosomal STR loci in a multiplex reaction using the AmpFlSTR Identifiler kit.37 PCR amplification was performed in a GeneAmp PCR System 9600 thermocycler37 following the cycling conditions described elsewhere.26, 27 Amplicons were separated by multi-capillary electrophoresis in an ABI Prism 3100 Genetic Analyzer37 and ABI program Genescan 500 LIZ was utilized as an internal size standard. The Genescan 3.7 program was employed to determine the fragment sizes and alleles were designated by comparison to an allelic ladder from the manufacturer using Genotyper 3.7 NT software.

Statistical and phylogenetic analyses

STR allelic frequencies were calculated utilizing the GENEPOP program in the web software v3.4.38 The Arlequin software package version 2.00039 was employed to estimate observed and expected heterozygosities (Ho and He, respectively) as well as to determine gene diversity indices (GDI). Several parameters of population genetics interest, including power of discrimination (PD), matching probability (MP), polymorphic information content (PIC), power of exclusion (PE) and typical paternity index (TPI) were obtained with the PowerStats program version 1.2.40, 41, 42

Allelic frequencies of the four collections in the current study as well as the reference populations (Table 1) were utilized to generate Neighbor Joining (NJ) dendrograms based on Nei's genetic distances for two different datasets involving 15 and 13 STR loci, respectively, using the PHYLIP v3.6 program.55 D2S1338 and D19S433 were excluded for the 13 loci analyses (from the 15 loci set) as the data for these loci were not reported for all reference populations. The robustness of the phylogenetic relationships established by the NJ tree was assessed using bootstrap analysis with 1000 reiterations. Correspondence Analyses (CA) were also performed with the two sets of 15 and 13 STR loci with the NTSYSpc-2.02i software.56

Table 1 Populations analyzed

Pairwise comparisons were conducted to ascertain genetic affinity between a given pair of populations with the Carmody program's G test57 involving 100 000 simulations. The Bonferroni correction was applied to account for the possibility of Type I errors resulting for the multiplicity of the tests performed. The DISPAN program58 was employed to compute inter-, intra- and total population variance (Gst, Hs and Ht, respectively) at the level of 13 STR loci. The populations analyzed were classified based on their geographical distributions as displayed in Table 1. In addition, DISPAN was utilized to calculate the average heterozygosity for each population.

Admixture estimations were generated by a Weighted Least Squares (WLS) method25, 59 using the Statistical Package for the Social Sciences (SPSS) 14.0 software. The WLS model calculates admixture proportions based on the following equation:

where pih is the frequency of the ith allele in the hybrid population, pij represents the frequency of the ith allele in the jth parental group (j=1, …., J), μj is the proportionate contribution of the jth parental gene pool to the hybrid population, and ∑jμj=1 (where, 0μj1).

Parental groups were partitioned according to geographical location as follows: Northeast Asia (Japan, Korea and Shaanxi), Southeast Asia (Chao Shan, Thailand, Malaysia and Philippines), South Asia (Pakistan, Punjab and Bangladesh) and Southwest Asia (Afghanistan, Iran and Iraq). Their contributions to the five Himalayan collections (Tibet, Tamang, Newar, Kathmandu and Bhutan) were examined across the 15 loci.

Results

Intra-population diversity

The allelic frequency distributions for Tibet, Tamang, Newar and Kathmandu are listed in Supplementary Tables 1 to 4. Combined Matching Probability (CMP), Combined Power of Exclusion (CPE), Combined Power of Discrimination (CPD) and Average GDI are provided in Supplementary Table 5. Loci D7S820 and THO1 in Kathmandu and D13S317 in Tibet were found to depart from Hardy–Weinberg equilibrium (HWE) expectations, however, these deviations were rendered statistically insignificant after applying the Bonferroni correction (α=0.05/15=0.0033). The highest GDI in Tibet is found at the FGA locus (0.8792) whereas the maximum values for this parameter are observed at D18S51 (0.8597) and D2S1338 (0.8854 and 0.8823) in Tamang, Newar and Kathmandu, respectively. Intra-population variance (Hs) values are presented in Supplementary Table 6. The Southwest Asians possess the highest intra-population variance (0.7801) followed by the Himalayan (0.7771) and Southeast Asian (0.7767) collections, all of which are higher than the all-population group (0.7739), whereas the Northeast Asian assemblage exhibits the lowest value (0.7713).

Inter-population diversity: 15 STR loci analyses

Phylogenetic analyses based on allelic frequencies were performed to investigate the genetic relationships between the four Himalayan collections and other geographically targeted populations using the set of 15 STR loci. Four separate aggregates are evident in the CA plot (Figure 2): both Northeast Asian and Himalayan clusters (except for Kathmandu and Newar) in the upper right quadrant, the Southeast Asian assemblage in the lower right portion and the South Asia/Southwest Asia cluster on the left side of the graph. Kathmandu plots intermediate between the South/Southwest Asian group and the Himalayan and Northeast Asian collections. Newar is an outlier near the perimeter of the upper left quadrant whereas Tibet and Tamang map close to each other within the Himalayan assemblage. In the NJ phylogram (Figure 4), the Himalayan groups occupy an intermediate position between the East and South/Southwest Asian populations. Tibet, Tamang and Bhutan form a separate clade whereas Newar branches between Kathmandu and the general population from Nepal.

Figure 2
figure 2

Correspondence Analysis (CA) employing 15 STR loci.

G-test results at the 15 STR loci level are presented in Table 2. Only the Kathmandu and Bangladesh pair displayed non-significant genetic differences (G=186.0376, P=0.1139) from a total of 171 pairwise population comparisons at α=0.05. However, after applying the Bonferroni correction (α=0.05/171=0.0002924) several comparisons yielded additional statistically insignificant co-relationships (Table 2). Pairwise analyses using the 13 STR loci dataset generated similar results to those using 15 loci with the exception of an additional statistically insignificant populations pair (Iran/Punjab) (data not shown).

Table 2 G-Test results for populations using 15 STR loci

Admixture proportions were generated for the five Himalayan populations, namely Tibet, Tamang, Newar, Kathmandu and Bhutan using Northeast Asia, Southeast Asia, South Asia and Southwest Asia as parental populations (Table 3). When examining the genetic contributions from the parental groups, Northeast Asia arises as the major donor to Tibet (63.4%), Tamang (59.7%) and Newar (44.7%) and also contributes considerable proportions of the Bhutan (41.1%) and Kathmandu (22.3%) gene pools. Bhutan (44.3%), on the other hand is mainly influenced by Southeast Asia whereas relatively low inputs from the same region were observed in Tamang (29.0%), Tibet (21.1%) and Kathmandu (5.4%). In contrast, Kathmandu (63.3%) and Newar (41.5%) are primarily affected by the South Asian group, whereas the latter impacts the other Himalayan populations only minimally (Tibet 2.7%) or not at all (Tamang, 0.0% and Bhutan, 0.0%). All of the Himalayan collections experienced similar levels of gene flow from Southwest Asia (9–15%).

Table 3 Admixture analysis using regional groups

Inter-population diversity: 13 CODIS core STR loci analyses

To compare our Himalayan populations to TB groups from Northeast India and other Asian populations, allelic frequencies from the 13 CODIS STR loci shared among 25 collections were employed to perform additional phylogenetic analyses. Three well delineated groupings are apparent in the CA plot (Figure 3): the Northeast Indian assemblage (except for the Naga) in the lower right quadrant, the Southwest Asians with some South Asian populations in the lower left portion and the Himalayan/Northeast/Southeast Asian aggregate (except for Kathmandu and Newar) in the upper half of the graph. The NJ dendrogram (Figure 5) supports the information provided by the CA plot with the exception of three Himalayan groups (Tibet, Tamang and Bhutan) which form a sister clade with the Northeast Indian populations. Interestingly, populations within this Himalayan and Northeast Indian cluster belong to the same TB language subfamily.

Figure 3
figure 3

Correspondence Analysis (CA) using 13 STR loci.

Inter- and total population variance (Gst and Ht, respectively) are reported in Supplementary Table 6. South Asia displays the highest Gst (0.0222) while also sharing the greatest Ht values (0.7894) with the All-population group. In contrast, Northeast Asia exhibits the lowest Gst and Ht diversities (0.0036 and 0.7740, respectively). The Himalayan populations possess intermediate Gst and Ht values (0.0120 and 0.7811, respectively).

Discussion

In this study, 15 autosomal STR loci were typed in three Nepalese populations (Tamang, Newar and Kathmandu) and in a general collection from Tibet to investigate their genetic ancestry and phylogenetic relationships to other TB communities and worldwide populations. This work improves on an earlier study54 by examining ethnic groups from Nepal that are anthropologically well-defined. Furthermore, this report complements previous Y-chromosome data1 thereby providing a comprehensive analysis of the genetic diversity in the Himalayas.

On average, the Himalayan populations (Newar, Kathmandu, Tamang and Tibet) possess 126 alleles whereas Northeast, Southeast and the South Asian populations examined in this study average 151, 140 and 137 allelic variants, respectively. The lower genetic diversity of the Himalayan collections is also reflected in their relatively reduced average heterozygosity values (0.7862) when compared to those of Northeast Asia (0.7890), Southeast Asia (0.7907) and South Asia (0.8009). Of the four, Tamang displays the lowest genetic variance reflected in both its average gene diversity index value (0.7632) and average heterozygosity value (0.7702), a characteristic echoed in its limited Y-chromosomal diversity.1

The inter-population diversity (Gst) (Supplementary Table 6) among the Himalayan cluster (0.0120) is considerably higher than in Northeast (0.0036), Southwest (0.0053) and Southeast Asian (0.0068) populations but is lower than among the South Asian collections (0.0222) and the All-populations group (0.0196). The concurrence of limited heterozygosity and elevated Gst value in the Himalayan populations could be results of multiple genetic sources, genetic drift and/or founder effect. In addition, selective pressure and adaptation to high altitudes, possibly in combination with inbreeding and patrilocality, could also promote homozygosity and genetic differences among the populations. The relatively high Gst value observed among the South Asians is also reflected in the disperse partitioning of the Northeast Indian populations in the CA plot (Figure 3) and may reflect known socio-cultural and genetic barriers. High degree of genetic differentiation resulting from various source populations may account for the greater variance among Himalayan populations in comparison to the Northeast, Southeast and Southwest Asian assemblages.

It is noteworthy that all three Nepalese groups not only exhibit considerable genetic diversity among themselves but also with respect to the general population of Nepal (Figures 2 and 3). Kathmandu plots closer to the South Asian groups while still maintaining genetic proximity with the Himalayan and Northeast Asian clusters (Figures 2 and 3). Pairwise G-test comparisons between Kathmandu and Bangladesh (G=186.0376, P=0.1139) and Kathmandu and Pakistan (G=213.5188, P=0.0014) are statistically insignificant, after application of Bonferroni correction, indicating some degree of genetic homogeneity between these South Asian and Nepalese populations. Although Newar segregates from all other populations at the periphery of the upper left quadrant in the 15 loci CA graph (Figure 2), its location is intermediate between the South Asia and other Himalayan collections in the NJ phylogram (Figure 4). It is possible that the Newari population (an ethnic minority) has been subject to genetic isolation and drift generating this divergent phylogenetic profile. Conversely, genetic impacts from distinct source populations may have contributed to Newar's unique genetic partitioning. The latter possibility is also reflected in a previous study19 based on 11 genetic markers (blood groups, red cell enzyme and serum proteins) in which Newaris were found to cluster with two geographically distant Manipuri groups from Northeast India in the NJ tree rather than with Tamang and Gurung, both of Nepalese descent.

Figure 4
figure 4

Neighbor Joining (NJ) tree based on Nei's genetic distances generated using allele frequencies from the 15 STR loci. The numbers at the nodes represent bootstrap values estimated from 1000 replications.

The admixture profiles (Table 3) reveal a substantial proportion of South Asian genes (63.3%) in Kathmandu as compared to Northeast Asia (22.3%), supporting the relationships illustrated by both the G test and CA plot. Newar, on the other hand, experienced similar contributions from both regions (44.7 vs 41.5%), possibly accounting for its equidistant positioning to these groups of populations in the CA plot (Figure 3) and the NJ tree (Figure 4). The South Asian influence in the Nepalese populations may be associated with the entry of Aryans from the Indian plains who introduced the Indo-European language (Nepali) in the Kathmandu valley. A recent mtDNA study10 also reported reciprocal maternal gene flow between North India and Nepal. These results are consistent with the elevated levels of Y-haplogroup R in Newar (62.1%) and Kathmandu (46.7%), which are most likely derived from South Asia, particularly North India, given the geographic vicinity as well as the historical and socio-cultural affinities shared between these two neighboring regions.1 In contrast, Tamang and Tibet exhibit minimal percentages of Y-haplogroup R (8.8 and 2.5%, respectively), indicating that the Himalayas served as a formidable orographic barrier to gene flow from the south.1 Findings from the current investigation lend support to the aforementioned statement as admixture results reveal a null contribution from South Asia to both Tamang and Bhutan and only a minor genetic impact onto the Tibetan collection (2.7%). The absence of the South Asian signature in the gene pools of Tamang and Bhutan may be the result of geographic isolation and/or founder effects from another source population(s).

Close genetic ties have been reported between the Tamang and Tibet.1 It is likely that Tamangs are descendants of Tibetans who migrated south and settled in the southern region of the Himalayan range.1 This affinity is reflected in both CA plots (Figures 2 and 3) and NJ dendrograms (Figures 4 and 5). The Tibetan connection to the Tamang is also evident in their shared cultural and religious practices. The partitioning of these two populations with Bhutan and their proximity to the general collection from Nepal (Figures 2, 3, 4 and 5) may be associated with Neolithic migrants carrying Y-haplogroup O3a5-M134, an East Asian-specific marker, shared among TB populations.1, 3, 4, 9, 60 The Himalayan populations, with the exception of Newar and Kathmandu, segregate close to the Northeast Asian cluster in agreement with the admixture analyses results (Table 3). Northeast Asia is the major contributor to both Tibet (63.4%) and Tamang (59.7%) whereas Newar (44.7%) and Bhutan (41.1%) received equivalent percentages, followed by Kathmandu (22.3%). These results corroborate studies indicating a shared common ancestry between Tibet and the Northeast Asian collections of Japan and Korea by a variety of marker systems, including classical,61, 62 autosomal,63 Y-chromosome1, 12, 64, 65 and mtDNA.12, 64, 66, 67

Figure 5
figure 5

Neighbor Joining (NJ) tree based on Nei's genetic distances generated using allele frequencies from the 13 CODIS core STR loci. The numbers at the nodes represent bootstrap values estimated from 1000 replications.

More than half of the Tibetan men possess the YAP polymorphic Alu insertion in their Y-chromosome which is believed to have originated in Central Asia,1, 4, 11, 14 although its source remains highly debated.64, 68, 69 In this study, however, given the lack of representative Central Asian populations due to the paucity of the data available from the region, no clear connections were made between Tibet and its possible Central Asian genetic contributors. Afghanistan is the sole Central Asian collection included in the analyses and appears to make no contributions to any of the Himalayan groups except for a minor influence in Kathmandu (12.9%).

To evaluate the genetic relationships between the Himalayan collections and the neighboring TB-speaking populations at the regional level, six Northeast Indian TB groups were included in the phylogenetic and statistical analyses performed using the 13 core CODIS STR loci. These Northeast Indian TB groups map distantly from both the Himalayan and East Asian populations in the CA graph (Figure 3), inconsistent with previous Y-chromosome and mtDNA studies which report a high degree of genetic homogeneity between Himalayan and Northeast Indian TB groups.3, 4, 9, 70 The discrepancy observed between Y-chromosome and microsatellite polymorphisms in the Northeast Indian TB groups may be explained by a male founder effect from Northeast Asia and their subsequent genetic isolation for an extended period of time following their arrival.9

Altogether, our results suggest a Northeast Asian ancestry for the Himalayan populations with subsequent genetic admixture in Kathmandu and Newar populations from South Asia. South Asian influences in Tibet and Tamang are negligible most likely due to the natural barrier presented by the Himalayas.1 Tamang, Tibet and Bhutan display close genetic affiliations in all analyses possibly indicating a shared common ancestry. The biparental markers examined in this study reveal unique genetic profiles for the Northeast Indian TB groups, which are distinct from their Himalayan counterparts implying limited gene flow, geographic isolation and/or founder effects.

References

  1. Gayden, T., Cadenas, A. M., Regueiro, M., Singh, N. B., Zhivotovsky, L. A., Underhill, P. A. et al. The Himalayas as a directional barrier to gene flow. Am. J. Hum. Genet. 80, 884–894 (2007).

    CAS  Article  Google Scholar 

  2. Gordon, R. G. Ethnologue: Languages of the World, 15th edn (SIL International, Dallas, 2005).

    Google Scholar 

  3. Su, B., Xiao, J., Underhill, P., Deka, R., Zhang, W., Akey, J. et al. Y-Chromosome evidence for a northward migration of modern humans into Eastern Asia during the last Ice Age. Am. J. Hum. Genet. 65, 1718–1724 (1999).

    CAS  Article  Google Scholar 

  4. Su, B., Xiao, C., Deka, R., Seielstad, M. T., Kangwanpong, D., Xiao, J. et al. Y chromosome haplotypes reveal prehistorical migrations to the Himalayas. Hum. Genet. 107, 582–590 (2000).

    CAS  Article  Google Scholar 

  5. van Driem, G. L. in Tibeto-Burman Phylogeny and Prehistory: Languages, Material Culture, and Genes (eds Bellwood, P. & Renfrew, C.) 233–249 (MacDonald Institute for Archaeological Research, University of Cambridge, United Kingdom, 2002).

    Google Scholar 

  6. van Driem, G. L. in The Peopling of East Asia: Putting Together Archaeology, Linguistics and Genetics (eds Sagart L., Blench. R. & Sanches-Mazas, A.) 81–106 (Routledge Curzon, Taylor and Francis group, London, 2005).

    Book  Google Scholar 

  7. Sengupta, S., Zhivotovsky, L. A., King, R., Mehdi, S. Q., Edmonds, C. A., Chow, C. E. et al. Polarity and temporality of high-resolution y-chromosome distributions in India identify both indigenous and exogenous expansions and reveal minor genetic influence of Central Asian pastoralists. Am. J. Hum. Genet. 78, 202–221 (2006).

    CAS  Article  Google Scholar 

  8. Sahoo, S., Singh, A., Himabindu, G., Banerjee, J., Sitalaximi, T., Gaikwad, S. et al. A prehistory of Indian Y chromosomes: evaluating demic diffusion scenarios. Proc. Natl Acad. Sci. USA 103, 843–848 (2006).

    CAS  Article  Google Scholar 

  9. Cordaux, R., Weiss, G., Saha, N. & Stoneking, M. The northeast Indian passageway: a barrier or corridor for human migrations? Mol. Biol. Evol. 21, 1525–1533 (2004).

    CAS  Article  Google Scholar 

  10. Thangaraj, K., Chaubey, G., Kivisild, T., Selvi Rani, D., Singh, V. K., Ismail, T. et al. Maternal footprints of Southeast Asians in North India. Hum. Hered. 66, 1–9 (2008).

    Article  Google Scholar 

  11. Qian, Y., Qian, B., Su, B., Yu, J., Ke, Y., Chu, Z. et al. Multiple origins of Tibetan Y chromosomes. Hum. Genet. 106, 453–454 (2000).

    CAS  Article  Google Scholar 

  12. Hammer, M. F., Karafet, T. M., Park, H., Omoto, K., Harihara, S., Stoneking, M. et al. Dual origins of the Japanese: common ground for hunter-gatherer and farmer Y chromosomes. J. Hum. Genet. 51, 47–58 (2006).

    Article  Google Scholar 

  13. Thangaraj, K., Singh, L., Reddy, A. G., Rao, V. R., Sehgal, S. C., Underhill, P. A. et al. Genetic affinities of the Andaman Islanders, a vanishing human population. Curr. Biol. 13, 86–93 (2003).

    CAS  Article  Google Scholar 

  14. Hammer, M. F., Spurdle, A. B., Karafet, T., Bonner, M. R., Wood, E. T., Novelletto, A. et al. The geographic distribution of human Y chromosome variation. Genetics 145, 787–805 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Ding, Y. C., Wooding, S., Harpending, H. C., Chi, H. C., Li, H. P., Fu, Y. X. et al. Population structure and history in East Asia. Proc. Natl Acad. Sci. USA 97, 14003–14006 (2000).

    CAS  Article  Google Scholar 

  16. Aldenderfer, M. & Yinong, Z. The prehistory of the Tibetan plateau to the seventh century A.D.: perspectives and research from China and the West since 1950. J. World. Prehist. 18, 1–55 (2004).

    Article  Google Scholar 

  17. Mastana, S. S., Murry, B., Sachdeva, M. P., Das, K., Young, D., Das, M.K. et al. Genetic variation of 13 STR loci in the four endogamous tribal populations of Eastern India. Forensic. Sci. Int. 169, 266–273 (2007).

    CAS  Article  Google Scholar 

  18. Maity, B., Nunga, S. C. & Kashyap, V. K. Genetic polymorphism revealed by 13 tetrameric and 2 pentameric STR loci in four Mongoloid tribal population. Forensic. Sci. Int. 132, 216–222 (2003).

    CAS  Article  Google Scholar 

  19. Kumar, V., Basu, D. & Reddy, B. M. Genetic heterogeneity in northeastern India: reflection of Tribe-Caste continuum in the genetic structure. Am. J. Hum. Biol. 16, 334–345 (2004).

    Article  Google Scholar 

  20. Krithika, S., Trivedi, R., Kashyap, V. K. & Vasulu, T. S. Genetic diversity at 15 microsatellite loci among the Adi Pasi population of Adi tribal cluster in Arunachal Pradesh, India. Leg. Med. (Tokyo) 7, 306–310 (2005).

    CAS  Article  Google Scholar 

  21. Krithika, S., Trivedi, R., Kashyap, V. K., Bharati, P. & Vasulu, T. S. Antiquity, geographic contiguity and genetic affinity among Tibeto-Burman populations of India: a microsatellite study. Ann. Hum. Biol. 33, 26–42 (2006).

    CAS  Article  Google Scholar 

  22. Kashyap, V. K., Chattopadhyay, P., Dutta, R. & Vasulu, T. S. Genetic structure and affinity among eight ethnic populations of Eastern India: based on 22 polymorphic DNA loci. Am. J. Hum. Biol. 16, 311–327 (2004).

    CAS  Article  Google Scholar 

  23. Parkin, E. J., Kraayenbrink, T., van Driem, G. L., Tshering Of Gaselo, K., de Knijff, P. & Jobling, M. A. 26-Locus Y-STR typing in a Bhutanese population sample. Forensic. Sci. Int. 161, 1–7 (2006).

    CAS  Article  Google Scholar 

  24. Parkin, E. J., Kraayenbrink, T., Opgenort, J. R., van Driem, G. L., Tuladhar, N. M., de Knijff, P. et al. Diversity of 26-locus Y-STR haplotypes in a Nepalese population sample: isolation and drift in the Himalayas. Forensic. Sci. Int. 166, 176–181 (2007).

    CAS  Article  Google Scholar 

  25. Perez-Miranda, A. M., Alfonso-Sanchez, M. A., Pena, J. A. & Herrera, R. J. Qatari DNA variation at a crossroad of human migrations. Hum. Hered. 61, 67–79 (2006).

    CAS  Article  Google Scholar 

  26. Shepard, E. M. & Herrera, R. J. Iranian STR variation at the fringes of biogeographical demarcation. Forensic. Sci. Int. 158, 140–148 (2006a).

    CAS  Article  Google Scholar 

  27. Shepard, E. M. & Herrera, R. J. Genetic encapsulation among Near Eastern populations. J. Hum. Genet. 51, 467–476 (2006b).

    Article  Google Scholar 

  28. Shepard, E. M., Chow, R. A., Suafo’a, E., Addison, D., Perez-Miranda, A. M., Garcia-Bertrand, R. L. et al. Autosomal STR variation in five Austronesian populations. Hum. Biol. 77, 825–851 (2005).

    CAS  Article  Google Scholar 

  29. Rowold, D. J. & Herrera, R. J. Inferring recent human phylogenies using forensic STR technology. Forensic. Sci. Int. 133, 260–265 (2003).

    CAS  Article  Google Scholar 

  30. Ying, B., Liu, T., Chen, G., Zhao, Z., Fan, H. & Wen, F. Genetic profile of two Tibetan populations from China by analysis of 15 STR loci. Hum. Biol. 78, 757–770 (2006).

    Article  Google Scholar 

  31. Yan, J., Shen, C., Li, Y., Yu, X., Xiong, X., Mu, H. et al. Genetic analysis of 15 STR loci on Chinese Tibetan in Qinghai province. Forensic. Sci. Int. 169, e3–e6 (2007).

    CAS  Article  Google Scholar 

  32. Ota, M., Droma, Y., Basnyat, B., Katsuyama, Y., Asamura, H., Sakai, H. et al. Allele frequencies for 15 STR loci in Tibetan populations from Nepal. Forensic. Sci. Int. 169, 234–238 (2007).

    CAS  Article  Google Scholar 

  33. Kang, L. L., Zhao, J., Liu, K. & Li, X. Allele frequencies of 15 STR loci of Tibetan lived in Tibet Lassa. Forensic. Sci. Int. 168, 236–240 (2007).

    CAS  Article  Google Scholar 

  34. Kang, L., Yuan, D., Yang, F., Liu, K. & Za, X. Genetic polymorphisms of 15 STR loci in two Tibetan populations from Tibet Changdu and Naqu, China. Forensic. Sci. Int. 169, 239–243 (2007).

    CAS  Article  Google Scholar 

  35. Kang, L. & Li, S. Allele frequencies of 15 STR loci of Luoba ethnic group in Tibet (Southwestern China). Forensic. Sci. Int. 155, 219–221 (2005).

    CAS  Article  Google Scholar 

  36. Antunez-de-Mayolo, G., Antunez-de-Mayolo, A., Antunez-de-Mayolo, P., Papiha, S. S., Hammer, M., Yunis, J. J. et al. Phylogenetics of worldwide human populations as determined by polymorphic Alu insertions. Electrophoresis 23, 3346–3356 (2002).

    CAS  Article  Google Scholar 

  37. Applied Biosystems. AmpFlSTR Identifiler PCR Amplification Kit User's Manual (Applied Biosystems, Foster City, CA, USA, 2001).

    Google Scholar 

  38. Raymon, M. & Rousset, F. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249 (1995).

    Article  Google Scholar 

  39. Schneider, S., Kueffer, J. M., Roessli, D. & Excoffier, L. Arlequin v. 2.000: A Software for Population Genetic Analysis (Genetics and Biometry Laboratory, University of Geneva, Geneva, 2000).

    Google Scholar 

  40. Jones, D. A. Blood samples: probability of discrimination. J. Forensic. Sci. Soc. 12, 355–359 (1972).

    CAS  Article  Google Scholar 

  41. Brenner, C. H. & Morris, J. W Proceedings for the International Symposium on Human Identification (Promega Corporation, Madison, 1990).

    Google Scholar 

  42. Tereba, A. Profiles in DNA (Promega Corporation, Madison, 1999).

    Google Scholar 

  43. Hashiyada, M., Itakura, Y., Nagashima, T., Nata, M. & Funayama, M. Polymorphism of 17 STRs by multiplex analysis in Japanese population. Forensic. Sci. Int. 133, 250–253 (2003).

    CAS  Article  Google Scholar 

  44. Kim, Y. L., Hwang, J. Y., Kim, Y. J., Lee, S., Chung, N. G., Goh, H. G. et al. Allele frequencies of 15 STR loci using AmpF/STR Identifiler kit in a Korean population. Forensic. Sci. Int. 136, 92–95 (2003).

    CAS  Article  Google Scholar 

  45. Wang, Z. Y., Yu, R. J., Wang, F., Li, X. S. & Jin, T. B. Genetic polymorphisms of 15 STR loci in Han population from Shaanxi (NW China). Forensic. Sci. Int. 147, 89–91 (2005).

    CAS  Article  Google Scholar 

  46. Hu, S. P., Yu, X. J., Liu, J. W. & Cai, K. L. Analysis of STR polymorphisms in the Chao Shan population in South China. Forensic. Sci. Int. 147, 93–95 (2005).

    CAS  Article  Google Scholar 

  47. Seah, L. H., Jeevan, N. H., Othman, M. I., Jaya, P., Ooi, Y. S., Wong, P. C. et al. STR data for the AmpFlSTR Identifiler loci in three ethnic groups (Malay, Chinese, Indian) of the Malaysian population. Forensic. Sci. Int. 138, 134–137 (2003).

    CAS  Article  Google Scholar 

  48. De Ungria, M. C. A., Roby, R. K., Tabbada, K. A., Rao-Coticone, S., Tan, M. M. & Hernandez, K. N. Allele frequencies of 19 STR loci in a Philippine population generated using AmpFlSTR multiplex and ALF singleplex systems. Forensic. Sci. Int. 152, 281–284 (2005).

    CAS  Article  Google Scholar 

  49. Rerkamnuaychoke, B., Rinthachai, T., Shotivaranon, J., Jomsawat, U., Siriboonpiputtana, T., Chaiatchanarat, K. et al. Thai population data on 15 tetrameric STR loci—D8S1179, D21S11, D7S820, CSF1PO, D3S1358, TH01, D13S317, D16S539, D2S1338, D19S433, vWA, TPOX, D18S51, D5S818 and FGA. Forensic. Sci. Int. 158, 234–237 (2006).

    CAS  Article  Google Scholar 

  50. Berti, A., Barni, F., Virgili, A., Iacovacci, G., Franchi, C., Rapone, C. et al. Autosomal STR frequencies in Afghanistan population. J. Forensic. Sci. 50, 1494–1496 (2005).

    CAS  PubMed  Google Scholar 

  51. Barni, F., Berti, A., Pianese, A., Boccellino, A., Miller, M. P., Caperna, A. et al. Allele frequencies of 15 autosomal STR loci in the Iraq population comparisons to other populations from the middle-eastern. Forensic. Sci. Int. 167, 87–92 (2007).

    CAS  Article  Google Scholar 

  52. Dobashi, Y., Kido, A., Fujitani, N., Susukida, R., Hara, M. & Oya, M. STR data for the AmpFlSTR Identifiler loci in Bangladeshi and Indonesian populations. Leg. Med. 7, 222–226 (2005).

    CAS  Article  Google Scholar 

  53. Kraaijenbrink, T., van Driem, G. L., Tshering of Gaselo, K. & de Knijff, P. Allele frequency distribution for 21 autosomal STR loci in Bhutan. Forensic. Sci. Int. 170, 68–72 (2007a).

    CAS  Article  Google Scholar 

  54. Kraaijenbrink, T., van Driem, G. L., Opgenort, J. R. M. L., Tuladhar, N. M. & de Knijff, P. Allele frequency distribution for 21 autosomal STR loci in Nepal. Forensic. Sci. Int. 168, 227–231 (2007b).

    CAS  Article  Google Scholar 

  55. Felsentein, J. Phylogeny Inference Package (PHYLIP) Version 3.6a3 (Department of Genetics, University of Washington, Seattle, 2002).

    Google Scholar 

  56. Rohlf, F. NTSYSpc (Exter Publishing, Setauket, NY, 2002).

    Google Scholar 

  57. Carmody, G. G-test (Carleton University, Ottawa, 1990).

    Google Scholar 

  58. Ota, T. DISPAN: Genetic Distance and Phylogenetic Analysis (Institute of Molecular Evolutionary Genetics, Pennsylvania State University, Pennsylvania, 1993).

    Google Scholar 

  59. Long, J. C., Williams, R. C., McAuley, J. E., Medis, R., Partel, R., Tregellas, W. M. et al. Genetic variation in Arizona Mexican Americans: estimation and interpretation of admixture proportions. Am. J. Phys. Anthropol. 84, 141–157 (1991).

    CAS  Article  Google Scholar 

  60. Black, M. L., Wise, C. A., Wang, W. & Bittles, A. H. Combining genetics and population history in the study of ethnic diversity in the People's Republic of China. Hum. Biol. 78, 277–293 (2006).

    CAS  Article  Google Scholar 

  61. Cavalli-Sforza, L. L., Menozzi, P. & Piazza, A. The History and Geography of Human Genes (Princeton University Press, Princeton, NJ, USA, 1994).

    Google Scholar 

  62. Nei, M. & Roychoudhury, A. K. Evolutionary relationships of human populations on a global scale. Mol. Biol. Evol. 10, 927–943 (1993).

    CAS  PubMed  Google Scholar 

  63. Chu, J. Y., Huang, W., Kuang, S. Q., Wang, J. M., Xu, J. J. & Chu, Z. T. Genetic relationship of populations in China. Proc. Natl Acad. Sci. USA 95, 11763–11768 (1998).

    CAS  Article  Google Scholar 

  64. Tajima, A., Hayami, M., Tokunaga, K., Juji, T., Matsuo, M., Marzuki, S. et al. Genetic origins of the Ainu inferred from combined DNA analyses of maternal and paternal lineages. J. Hum. Genet. 49, 187–193 (2004).

    CAS  Article  Google Scholar 

  65. Tajima, A., Pan, I. H., Fucharoen, G., Fucharoen, S., Matsuo, M., Tokunaga, K. et al. Three major lineages of Asian Y chromosomes: implications for the peopling of east and southeast Asia. Hum. Genet. 110, 80–88 (2002).

    CAS  Article  Google Scholar 

  66. Tanaka, M., Cabrera, V. M., Gonzalez, A. M., Larruga, J. M., Takeyasu, T., Fuku, N. et al. Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome. Res. 14, 1832–1850 (2004).

    CAS  Article  Google Scholar 

  67. Torroni, A., Miller, J. A., Moore, L. G., Zamudio, S., Zhuang, J., Droma, T. et al. Mitochondrial DNA analysis in Tibet: implications for the origin of the Tibetan population and its adaptation to high altitude. Am. J. Phys. Anthropol. 93, 189–199 (1994).

    CAS  Article  Google Scholar 

  68. Jin, L. & Su, B. Natives or immigrants: modern human origin in east Asia. Nat. Rev. Genet. 1, 126–133 (2000).

    CAS  Article  Google Scholar 

  69. Underhill, P. A. in The Peopling of East Asia: Putting Together Archaeology, Linguistics, and Genetics (eds. L. Sagart., R. Blench. & A. Sanchez-Mazas.) 301–319 (Routledge Curzon, Taylor and Francis group, London, 2004).

    Google Scholar 

  70. Wen, B., Xie, X., Gao, S., Li, H., Shi, H., Song, X. et al. Analyses of genetic structure of Tibeto-Burman populations reveals sex-biased admixture in southern Tibeto-Burmans. Am. J. Hum. Genet. 74, 856–865 (2004).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Diane J Rowold and Javier R Luis for their constructive criticism of the article, and Charlie Haz and Michael Solier for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rene J Herrera.

Additional information

Supplementary Information accompanies the paper on Journal of Human Genetics website (http://www.nature.com/jhg)

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gayden, T., Mirabal, S., Cadenas, A. et al. Genetic insights into the origins of Tibeto-Burman populations in the Himalayas. J Hum Genet 54, 216–223 (2009). https://doi.org/10.1038/jhg.2009.14

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/jhg.2009.14

Keywords

  • autosomal STRs
  • Himalayas
  • Nepal
  • Tibet
  • Tibeto-Burman

Further reading

Search

Quick links