* Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
Department of Biological Sciences, Louisiana State University, Baton Rouge
WE Informatik, Heinrich-Heine-Universitaet Duesseldorf, Duesseldorf, Germany
Department of Pediatrics, National University of Singapore, Singapore
Correspondence: E-mail: cordaux{at}lsu.edu.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key Words: northeast India humans genetic diversity Y chromosome mtDNA
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The northeastern tip of India, flanked in the north by the Himalayas and in the south by the Bay of Bengal, constitutes a unique narrow passageway that connects the Indian subcontinent to East Asia and Southeast Asia (fig. 1). It is thought to have been a crucial corridor for human migrations between these two subcontinental areas, including, perhaps, the first migrations from Africa towards East Asia and Australia more than 40,000 years ago (Nei and Roychoudhury 1993; Cavalli-Sforza, Menozzi, and Piazza 1994; Lahr and Foley 1994; Cann 2001).
|
A putative long history of migrations, coupled with diverse cultural influences as evidenced by the high linguistic diversity, would predict that northeast India has experienced extensive population interactions that have resulted in high genetic diversity within groups and heterogeneity among groups. To test this hypothesis, we analyzed Y-chromosome and mitochondrial DNA (mtDNA) variation in the Adi, Apatani, Nishi, and Naga tribal populations, sampled from diverse northeast Indian localities. They speak Tibeto-Burman languages and are also conversant in Indo-European languages, such as Hindi or Assamese (Singh 1998). Genetic variation in these groups was compared with that of other Indian and East/Southeast Asian groups. We find that, contrary to the prediction, northeast Indian groups show a striking genetic homogeneity both in terms of Y-chromosome and mtDNA variation, which was probably maintained over time by genetic isolation. In addition, northeast Indians show virtually no genetic admixture with other Indian groups, which has led to a remarkable genetic discontinuity between these groups. This suggests that the northeast Indian passageway was a geographic barrier to contacts between the Indian subcontinent and East/Southeast Asia, rather than a corridor, at least within the past millennia.
![]() |
Subjects and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Y Chromosome Typing
Fourteen slowly evolving Y-chromosome biallelic polymorphisms were typed. Markers M9, M17, M20, M52, M74, M89, M122, M124, M172, M175, RPS4Y, and YAP were typed as described (Hammer and Horai 1995; Kayser et al. 2000a, 2001, 2003; Ke et al. 2001; Cordaux et al. 2004). Markers M134 and M174 were typed by PCR-RFLP using the procedure described by Cordaux et al. (2004); primers and PCR conditions for these two markers are given in table 1. The nomenclature used is that of the Y-Chromosome Consortium 2003 (Jobling and Tyler-Smith 2003).
|
Statistical Analyses
The software package ARLEQUIN version 2.0 (Schneider, Roessli, and Excoffier 2000) was used to calculate Y-haplogroup diversity and Fst distances between pairs of populations and associated P values based on 1,000 permutations. The Mann-Whitney U test to compare diversity values was computed with STATISTICA. 2 tests to compare haplogroup frequency distributions was calculated in EXCEL (Microsoft). Analyses of molecular variance (AMOVA) were performed by use of ARLEQUIN, and the significance of variance components were tested with 10,000 permutations. Multidimensional scaling (MDS) analysis was performed by means of STATISTICA, based on Fst distances. Populations from northeast India were compared with 131 tribal and 24 caste south Indians (Cordaux et al. 2004), 72 west Indians, 66 north Indians, 31 east Indians (Kivisild et al. 2003), 46 Tibetans, 365 Han Chinese, 76 south Chinese (Su et al. 2000b), and 71 Southeast Asians (Su et al. 2000a). The Indian and East/Southeast Asian contributions to the northeast Indian Y-chromosome gene pool were estimated by use of (1) a phylogeographic approach (Cordaux et al. 2004) and (2) the program ADMIX version 2.0 (Dupanloup and Bertorelle 2001). The two parental populations were represented by the 324 Indian and 558 East/Southeast Asian individuals described above, and standard errors (SE) were calculated on the basis of 1,000 bootstraps.
The Y-STRs were recorded as haplotypes. ARLEQUIN was used to calculate (1) Y-STR haplotype diversity, and (2) mean pairwise differences (MPD), the mean number of mutational steps observed between all pairs of haplotypes in the sample. Variance in allele size distribution was calculated in EXCEL for each locus independently and then averaged across the five loci. A median-joining network connecting the different Y-STR haplotypes was constructed by utilizing the NETWORK version 3.1 software (Bandelt, Forster, and Rohl 1999). Locus-specific weights were given according to Kayser et al. (2000a, 2000b), so that loci with the highest mutation rates were given the lowest weights. Hence, DYS389I, DYS390, DYS391, DYS392, and DYS393 were given weights of 5, 1, 2, 10, and 10, respectively. In addition, Y-STR haplotypes were compared with 109 haplotypes from East, Southeast, and island Southeast Asia (Kayser et al. 2000a, 2003) to estimate the extent of haplotype sharing between these groups and northeast Indian groups.
A coalescence analysis of the 139 Y-STR haplotypes was performed by use of the BATWING version 1.0 software (Wilson, Weale, and Balding 2003). A two-phase population model was chosen, in which population size in the past was constant, and then experienced a period of exponential growth until the present. Thus, the demography of the population is defined by three parameters: initial population size, growth rate, and time since expansion. Details on the prior distribution characteristics used to model the three aforementioned demographic parameters are given in Kayser et al. (2000a, 2001). In brief, they cover a range of demographic scenarios that range from no growth (constant population size) to reasonable growth rates for human populations (Kayser et al. 2000a, 2001). Gamma-distributed prior distributions were assigned to the mutation rates of the five STR loci, adjusted to the corresponding estimates reported in Kayser et al. (2000b). A Markov chain Monte Carlo method was then used to generate approximate random samples for converting the prior distributions into posterior distributions, which, in turn, reflect the information contained in the data.
mtDNA Analyses
The ADMIX software was used to evaluate the Indian and East/Southeast Asian contributions to the northeast Indian mtDNA gene pool. The Indian parental population was represented by 560 tribal and nontribal individuals (Cordaux et al. 2003). The East/Southeast Asian parental population was represented by 742 individuals (see Cordaux et al. [2003] and references therein). Standard errors were estimated on the basis of 1,000 bootstraps. Fst distances based on mtDNA HV1 sequences were calculated in ARLEQUIN.
The 192 northeast Indian mtDNA sequences were also used to estimate expansion time (in mutational units), as implemented in ARLEQUIN. The expansion time t (in years) was then deduced using the relationship t =
/ 2u, where u is the mutation rate for the whole sequence. We used a mutation rate of 1.65 x 107/site/year (Ward et al. 1991) and estimated 95% confidence intervals on the basis of 1,000 bootstraps.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
|
|
|
|
|
|
With regard to mtDNA relationships, Cordaux et al. (2003) have shown that northeast Indian groups show closer affinities to East/Southeast Asians and are well differentiated from other nonnortheast Indian groups. An ADMIX analysis formally evaluating the East/Southeast Asian and Indian contributions to the northeast Indian mtDNA gene pool confirms this trend, in that East/Southeast Asians have largely (90%) (table 3) contributed present-day northeast Indian mtDNAs. The mtDNA results, thus, strikingly parallel the Y-chromosome data.
We estimated the expansion time to be 6.5 mutational units (95% confidence interval: 4.2 to 7.8), which yielded an expansion time t of 54,000 years (95% confidence interval: 35,000 to 64,000), based on 192 northeast Indian mtDNA sequences. This is in sharp contrast with the expansion time of approximately 1,400 years obtained from Y-STR data (table 6, fig. 5).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The demographic scenario suggested by Y-STR variation involves a founder effect; that is, present-day northeast Indian males are derived from a small number of migrants from an East Asian source population. Alternatively, they may have gone through bottlenecks after they reached India. This is supported by (1) the low Y-chromosome diversity (both at haplogroup and STR levels), (2) the fact that only four closely related Y-STR haplotypes encompass 80% of all haplotypes, and (3) all haplotypes are closely related to the four major haplotypes. Moreover, the single Y-haplogroup O-M134 accounts for 85% of all Y-lineages in northeast India, whereas the frequency of O-M134 in the putative source population is approximately 30%. The fact that all northeast Indian populations analyzed consistently show these trends points to a founder effect during the colonization of northeast India rather than to bottlenecks. This is because bottlenecks subsequent to the colonization of northeast India would not be expected to affect all populations in the same way, unless a bottleneck happened right after the founding population arrived in northeast India, before the separation of the different groups. However, a bottleneck immediately after arriving in northeast India would essentially be the same as a founder event, for all practical purposes, because it means the reduction in diversity happened either when protoTibeto-Burman speakers left east Asia or right when they got to northeast India, not that they were in northeast India for a long time before going through bottlenecks.
This conclusion has important implications because, in the case of separate bottlenecks occurring in the northeast Indian populations, the start of the demographic expansion would provide an indication on the timing of the bottlenecks, not on the timing of the migration to northeast India. However, in the case of a founder effect associated with the colonization of northeast India, the demographic expansion took place immediately or shortly after the colonization, and, hence, the start of the demographic expansion probably represents a good approximation of the time of the migration to northeast India. Our coalescence analysis suggests that the expansion of Tibeto-Burman speakers to northeast India most likely took place within the past 4,200 years, which corresponds to the upper limit of the 95% probability interval of the time since expansion (table 6 and fig. 5B). A fairly recent separation of northeast Indians from their East Asian source is further supported by the low differentiation of the different northeast Indian groups based on Y-haplogroup frequencies and the extensive sharing of Y-STR haplotypes with East Asians.
Other Y-chromosome evidence, based on 607 individuals speaking Sino-Tibetan languages (to which the Tibeto-Burman family belongs), suggested that the cradle of Sino-Tibetan speakers was in China, perhaps in the Yellow River basin (Su et al. 2000b). Based on the allele size variance of three Y-STRs, Su et al. (2000b) inferred that protoTibeto-Burman speakers left China 5,000 to 6,000 years ago, which is consistent with archaeological and linguistic evidence (Wu and Poirier 1995; Etler 1996) and with the present study. Indeed, almost all northeast Indian Tibeto-Burman Y chromosomes can be assigned an East/Southeast Asian origin, and the admixture with other Indian groups is negligible. This suggests that Tibeto-Burman speakers may have been the first settlers of this area, which is plausible, given the inhospitable topological, climatic, and environmental conditions of the region. Alternatively, Tibeto-Burman newcomers may have found the land already inhabited, in which case they largely replaced the previous inhabitants of northeast India. Possible preTibeto-Burman inhabitants of northeast India are Austro-Asiatic speakers, who nowadays live both west and east of northeast India (Ruhlen 1991) but are represented in northeast India by a single group (the Khasi in Meghalaya [Singh 1998]). The archaeological record of northeast India provides little evidence for pre-Neolithic settlements of the area (Misra 2001), which could be interpreted as favoring the former hypothesis. However, the northeast Indian archaeological record is very poor, which might explain the paucity of pre-Neolithic evidence.
In addition, the Indo-European component of Tibeto-Burman Y chromosomes is remarkably low (3%), given that although the study groups are primarily Tibeto-Burman speakers, they are also conversant with Indo-European languages. This implies that the "Indo-Europeanization" of northeast India, which is an ongoing process (Masica 1991), is mainly a cultural process. This situation contrasts with southern India, where Indo-European speakers were integrated in nonIndo-European speech communities (Masica 1991) and where Y-chromosome markers typical of Indo-European speakers have been detected in Dravidian-speaking tribal groups (Bamshad et al. 2001; Ramana et al. 2001; Cordaux et al. 2004).
mtDNA Variation in Northeast India
Y-chromosome variation is paternally-inherited and, thus, only reflects male genetic history. How does it compare with mtDNA variation, the female equivalent of the Y chromosome? Y-chromosome and mtDNA variation differ in northeast Indian groups in that reduced Y-chromosome diversity contrasts with high mtDNA diversity, as opposed to other Indian tribal groups (Cordaux et al. 2003; present study). This may be attributable at least in part to the patrilocal residence rule of these groups (in which women move to their husband's residence after marriage), because this leads to diverse Y chromosomes entering a population at a lower rate than mtDNA (Seielstad, Minch, and Cavalli-Sforza 1998; Oota et al. 2001). However, under this scenario, one expects to find a correlation between Y chromosomes and geographic distances and no correlation between mtDNA and geographic distances (Seielstad, Minch, Cavalli-Sforza 1998). Nevertheless, northeast Indian groups do not adhere to this trend (mtDNA: r2 = 0.77, P = 0.55; Y chromosome: r2 = 0.03, P = 0.44), perhaps because of their low Y-chromosome and mtDNA differentiation or because of the relatively low number of populations compared. Another factor that may have contributed to elevation of mtDNA but not Y-chromosome diversity is gene flow with Indian groups, because mtDNA does indicate about 10% genetic contribution from India (table 3). Alternatively, the different patterns of Y-chromosome and mtDNA diversity observed in northeast India may be best explained by a male-specific founder effect during the colonization of northeast India. This scenario actually finds support in the fact that mtDNA evidence suggests an expansion time approximately 50,000 years ago. This estimate is very similar to that deduced for most human populations (Excoffier and Schneider 1999). Thus, it is more parsimonious to infer that the mtDNA expansion time relates to the human expansion out of Africa, rather than to multiple independent and simultaneous expansions during the colonization of each geographic area. The discrepancy between mtDNA and Y-STR expansion times can be explained by the different mutation rates for each system, which allows them to capture different demographic events during human evolution. It is noteworthy that Excoffier and Schneider (1999) found that a recent loss of diversity (through bottleneck or founder effect) can erase signals of past population expansion. As the northeast Indian mtDNA gene pool carries a signal of expansion approximately 50,000 years ago (as do the mtDNA gene pool of most other populations), it is reasonable to conclude that northeast Indian females did not experience any substantial recent loss of genetic diversity, contrary to northeast Indian males.
Similar to the Y-chromosome evidence, mtDNA evidence clearly indicates close genetic affinities between northeast Indian and east Asian groups (Cordaux et al. 2003) with hardly any contribution from nonnortheast Indians to the highly homogeneous northeast Indian mtDNA gene pool. In sum, both Y-chromosome and mtDNA evidence indicate that northeast Indian groups have remained genetically isolated for centuries, without admixing with their close Indian neighbors. The high incidence of genetic traits such as color blindness (e.g., which occurs at more than 10% in Apatani [Jaswal 1975; Singh 1998]) suggests considerable levels of inbreeding in these groups and provides additional evidence for their genetic isolation.
Was Northeast India a Barrier or Corridor for Human Migrations?
The findings of the present study are surprisingly contradictory with the initial prediction of high genetic heterogeneity and diversity in northeast India, based on the fact that the northeast Indian passageway is an important linguistic contact zone, and it is generally believed to have been a key area for migrations between India and East/Southeast Asia (see Introduction [Basu et al. 2003]). Genetic analyses of other postulated corridors have shown evidence of clinal variation and/or admixture between populations located adjacent to corridors such as the Nile River Valley (Krings et al. 1999), central Asia (Karafet et al. 2001; Wells et al. 2001; Zerjal et al. 2002; Comas et al. 2004), and eastern Indonesia (Kayser et al. 2000a).
However, there is a strikingly high genetic homogeneity in northeast India, coupled with a remarkable discontinuity in both Y-chromosome and mtDNA variation between northeast India and the rest of India. In the light of the present genetic evidence, we suggest that the northeast Indian passageway acted as a geographic barrier between the Indian subcontinent and East/Southeast Asia, rather than as an important corridor connecting these two major subcontinental areas, at least since the arrival of Tibeto-Burman speakers in northeast India.
Several recent studies have emphasized that the mtDNA and Y-chromosome gene pools of the Indian subcontinent and East/Southeast Asia are related but overall fairly distinct (Kivisild et al. 1999, 2003; Bamshad et al. 2001; Forster et al. 2001; Roychoudhury et al. 2001; Cordaux et al. 2003, 2004). The relatedness of the two gene pools may be interpreted as an indication that the northeast Indian passageway acted as a corridor between the Indian subcontinent and East/Southeast Asia during the initial settlement of the latter area. However, the distinctiveness of the same gene pools argues against considerable gene flow between the two areas for a long period of time, perhaps as long as 30,000 years, as suggested by mtDNA evidence (Forster et al. 2001). Taken together with the evidence presented in this study, we suggest that the northeast Indian passageway mainly acted as a barrier to migrations during most of modern human history.
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
![]() |
Literature Cited |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Abbi, A. 1991. Reduplication in south Asian languages: an areal, typological and historical study. Allied Publishers, New Delhi.
Bamshad, M., T. Kivisild, and W. S. Watkins, et al. (18 co-authors). 2001. Genetic evidence on the origins of Indian caste populations. Genome Res. 11:994-1004.
Bandelt, H. J., P. Forster, and A. Röhl. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16:37-48.[Abstract]
Basu, A., N. Mukherjee, and S. Roy, et al. (12 co-authors). 2003. Ethnic India: a genomic view, with special reference to peopling and structure. Genome Res. 13:2277-2290.
Cann, R. L. 2001. Genetic clues to dispersal in human populations: retracing the past from the present. Science 291:1742-1748.
Cavalli-Sforza, L. L., P. Menozzi, and A. Piazza. 1994. History and geography of human genes. Princeton University Press, Princeton, NJ.
Clark, V. J., S. Sivendren, N. Saha, G. R. Bentley, R. Aunger, S. M. Sirajuddin, and M. Stoneking. 2000. The 9-bp deletion between the mitochondrial lysine tRNA and COII genes in tribal populations of India. Hum. Biol. 72:273-285.[ISI][Medline]
Comas, D., S. Plaza, R. S. Wells, N. Yuldaseva, O. Lao, F. Calafell, and J. Bertranpetit. 2004. Admixture, migrations, and dispersals in Central Asia: evidence from maternal DNA lineages. Eur. J. Hum. Genet. 12:495-504.[CrossRef][ISI][Medline]
Cordaux, R., R. Aunger, G. Bentley, I. Nasidze, S. M. Sirajuddin, and M. Stoneking. 2004. Independent origins of Indian caste and tribal paternal lineages. Curr. Biol. 14:231-235.[ISI][Medline]
Cordaux, R., N. Saha, G. R. Bentley, R. Aunger, S. M. Sirajuddin, and M. Stoneking. 2003. Mitochondrial DNA analysis reveals diverse histories of tribal populations from India. Eur. J. Hum. Genet. 11:253-264.[CrossRef][ISI][Medline]
Dupanloup, I., and G. Bertorelle. 2001. Inferring admixture proportions from molecular data: extension to any number of parental populations. Mol. Biol. Evol. 18:672-675.
Etler, D. A. 1996. The fossil evidence for human evolution in Asia. Annu. Rev. Anthropol. 25:275-301.[CrossRef][ISI]
Excoffier, L., and S. Schneider. 1999. Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions? Proc. Natl. Acad. Sci. USA 96:10597-10602.
Forster, P., A. Torroni, C. Renfrew, and A. Röhl. 2001. Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol. Biol. Evol. 18:1864-1881.
Hammer, M. F., and S. Horai. 1995. Y chromosomal DNA variation and the peopling of Japan. Am. J. Hum. Genet. 56:951-962.[ISI][Medline]
Jaswal, I. J. S. 1975. Anomalous color vision among three tribes of Arunachal Pradesh, India. Anthropologist 22:60-64.
Jobling, M. A., and C. Tyler-Smith. 2003. The human Y-chromosome: an evolutionary marker comes of age. Nat. Rev. Genet. 4:598-612.[CrossRef][ISI][Medline]
Karafet, T., L. Xu, R. Du, W. Wang, S. Feng, R. S. Wells, A. J. Redd, S. L. Zegura, and M. F. Hammer. 2001. Paternal population history of East Asia: sources, patterns, and microevolutionary processes. Am. J. Hum. Genet. 69:615-628.[CrossRef][Medline]
Kayser, M., S. Brauer, G. Weiss, W. Schiefenhövel, P. A. Underhill, P. Shen, P. Oefner, M. Tomaseo-Ponzetta, and M. Stoneking. 2003. Reduced Y-chromosome, but not mitochondrial DNA, diversity in human populations from West New Guinea. Am. J. Hum. Genet. 72:281-302.[CrossRef][ISI][Medline]
Kayser, M., S. Brauer, G. Weiss, W. Schiefenhövel, P. A. Underhill, and M. Stoneking. 2001. Independent histories of human Y chromosomes from Melanesia and Australia. Am. J. Hum. Genet. 68:173-190.[CrossRef][ISI][Medline]
Kayser, M., S. Brauer, G. Weiss, P. A. Underhill, L. Roewer, W. Schiefenhövel, and M. Stoneking. 2000a. Melanesian origin of Polynesian Y chromosomes. Curr. Biol. 10:1237-1246.[CrossRef][ISI][Medline]
Kayser, M., A. Caglia, and D. Corach, et al. (30 co-authors). 1997. Evaluation of Y-chromosomal STRs: a multicenter study. Int. J. Legal Med. 110:125-133.[CrossRef][ISI][Medline]
Kayser, M., L. Roewer, and M. Hedman, et al. (14 co-authors). 2000b. Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome revealed by direct observation in father/son pairs. Am. J. Hum. Genet. 66:1580-1588.[CrossRef][ISI][Medline]
Ke, Y., B. Su, and X. Song, et al. (23 co-authors). 2001. African origin of modern humans in east Asia: a tale of 12,000 Y chromosomes. Science 292:1151-1152.
Kivisild, T., M. J. Bamshad, and K. Kaldma, et al. (14 co-authors). 1999. Deep common ancestry of Indian and western-Eurasian mitochondrial DNA lineages. Curr. Biol. 9:1331-1334.[CrossRef][ISI][Medline]
Kivisild, T., S. Rootsi, and M. Metspalu, et al. (18 co-authors). 2003. The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations. Am. J. Hum. Genet. 72:313-332.[CrossRef][ISI][Medline]
Krings, M., A. H. Salem, and K. Bauer, et al. (13 co-authors). 1999. MtDNA analysis of Nile River Valley populations: a genetic corridor or barrier for migration? Am. J. Hum. Genet. 64:1166-1176.[CrossRef][ISI][Medline]
Lahr, M. M., and R. Foley. 1994. Multiple dispersals and modern human origins. Evol. Anthropol. 3:48-60.
Masica, C. P. 1991. The Indo-European languages. Cambridge University Press, Cambridge, UK.
Misra, V. N. 2001. Prehistoric human colonization of India. J. Biosci. 26:491-531.[ISI][Medline]
Nei, M., and A. K. Roychoudhury. 1993. Evolutionary relationships of human populations on a global scale. Mol. Biol. Evol. 10:927-943.[Abstract]
Oota, H., W. Settheetham-Ishida, D. Tiwawech, T. Ishida, and M. Stoneking. 2001. Human mtDNA and Y-chromosome variation is correlated with matrilocal vs. patrilocal residence. Nat. Genet. 29:20-21.[CrossRef][ISI][Medline]
Quintana-Murci, L., C. Krausz, T. Zerjal, and T , et al. (13 co-authors). 2001. Y-chromosome lineages trace diffusion of people and languages in southwestern Asia. Am. J. Hum. Genet. 68:537-542.[CrossRef][ISI][Medline]
Ramana, G. V., B. Su, L. Jin, L. Singh, N. Wang, P. Underhill, and R. Chakraborty. 2001. Y-chromosome SNP haplotypes suggest evidence of gene flow among caste, tribe, and the migrant Siddi populations of Andhra Pradesh, South India. Eur. J. Hum. Genet. 9:695-700.[CrossRef][ISI][Medline]
Roychoudhury, S., S. Roy, A. Basu, R. Banerjee, H. Vishwanathan, M. V. Usha Rani, S. K. Sil, M. Mitra, and P. P. Majumder. 2001. Genomic structures and population histories of linguistically distinct tribal groups of India. Hum. Genet. 109:339-350.[CrossRef][ISI][Medline]
Ruhlen, M. 1991. A guide to the world's languages, Vol 1. Stanford University Press, Stanford, Calif.
Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequin ver. 2.000: a software for population genetics data analysis. Genetics and Biochemistry laboratory, University of Geneva, Switzerland.
Seielstad, M. T., E. Minch, and L. L. Cavalli-Sforza. 1998. Genetic evidence for a higher female migration rate in humans. Nat. Genet. 20:278-280.[CrossRef][ISI][Medline]
Singh, K. S. 1998. People of India: India's communities, Vol IV-VI. Oxford University Press, Delhi, India.
Su, B., L. Jin, and P. Underhill, et al. (11 co-authors). 2000a. Polynesian origins: insights from the Y chromosome. Proc. Natl. Acad. Sci. USA 97:8225-8228.
Su, B., C. Xiao, and R. Deka, et al. (11 co-authors). 2000b. Y chromosome haplotypes reveal prehistorical migrations to the Himalayas. Hum. Genet. 107:582-590.[CrossRef][ISI][Medline]
Underhill, P. A., G. Passarino, A. A. Lin, P. Shen, M. M. Lahr, R. A. Foley, P. J. Oefner, and L. L. Cavalli-Sforza. 2001. The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann. Hum. Genet. 65:43-62.[CrossRef][ISI][Medline]
Ward, R. H., B. L. Frazier, K. Dew-Jager, and S. Pääbo. 1991. Extensive mitochondrial diversity within a single Amerindian tribe. Proc. Natl. Acad. Sci. USA 88:8720-8724.[Abstract]
Wells, R. S., N. Yuldasheva, and R. Ruzibakiev, et al. (27 co-authors). 2001. The Eurasian heartland: a continental perspective on Y-chromosome diversity. Proc. Natl. Acad. Sci. USA 98:10244-10249.
Wilson, I., M. Weale, and D. Balding. 2003. Inferences from DNA data: population histories, evolutionary processes and forensic match probabilities. J. Roy. Stat. Soc. A 166:155-188.[CrossRef][ISI]
Wu, X. Z., and F. E. Poirier. 1995. Human evolution in China. Oxford University Press, Oxford, UK.
Zerjal, T., R. S. Wells, N. Yuldasheva, R. Ruzibakiev, and C. Tyler-Smith. 2002. A genetic landscape reshaped by recent events: Y-chromosomal insights into central Asia. Am. J. Hum. Genet. 71:466-482.[CrossRef][Medline]