Gene Flow from the Indian Subcontinent to Australia
2002; Elsevier BV; Volume: 12; Issue: 8 Linguagem: Inglês
10.1016/s0960-9822(02)00789-3
ISSN1879-0445
AutoresAlan J. Redd, June Roberts-Thomson, Tatiana M. Karafet, Michael J. Bamshad, Lynn B. Jorde, J.M. Naidu, Bruce Walsh, Michael F. Hammer,
Tópico(s)Genomics and Phylogenetic Studies
ResumoPhenotypic similarities between Australian Aboriginal People and some tribes of India were noted by T.H. Huxley during the voyage of the Rattlesnake (1846–1850) [1Huxley T.H. On the geographical distribution of the chief modifications of mankind.Ethnol. Soc. J. (Lond.). 1870; 2: 404-412Google Scholar]. Anthropometric studies by Birdsell [2Birdsell J.B. Microevolutionary Patterns in Aboriginal Australia. Oxford University Press, Oxford1993Google Scholar] led to his suggestion that a migratory wave into Australia included populations with affinities to tribal Indians. Genetic evidence for an Indian contribution to the Australian gene pool is contradictory; most studies of autosomal markers have not supported this hypothesis ([3Kirk R.L. Thorne A.G. The Origin of the Australians. Humanities Press, New Jersey1976Google Scholar, 4Nei M. Roychoudhury A.K. Evolutionary relationships of human populations on a global scale.Mol. Biol. Evol. 1993; 10: 927-943PubMed Google Scholar, 5Cavalli-Sforza L.L. Menozzi P. Piazza A. The History and Geography of Human Genes. Princeton University Press, Princeton1994Google Scholar]; [6Redd A.J. Stoneking M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations.Am. J. Hum. Genet. 1999; 65: 808-828Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar] and references therein). On the other hand, affinities between Australian Aboriginal People and southern Indians were suggested based on maternally inherited mitochondrial DNA [6Redd A.J. Stoneking M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations.Am. J. Hum. Genet. 1999; 65: 808-828Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar]. Here, we show additional DNA evidence in support of Huxley's hypothesis of an Indian-Australian connection using single-nucleotide polymorphisms (SNPs) and short tandem repeats (STRs) on the nonrecombining portion of the Y chromosome (NRY). Phylogenetic analyses of STR variation associated with a major Australian SNP lineage indicated tight clustering with southern Indian/Sri Lankan Y chromosomes. Estimates of the divergence time for these Indian and Australian chromosomes overlap with important changes in the archaeological and linguistic records in Australia. These results provide strong evidence for an influx of Y chromosomes from the Indian subcontinent to Australia that may have occurred during the Holocene. Phenotypic similarities between Australian Aboriginal People and some tribes of India were noted by T.H. Huxley during the voyage of the Rattlesnake (1846–1850) [1Huxley T.H. On the geographical distribution of the chief modifications of mankind.Ethnol. Soc. J. (Lond.). 1870; 2: 404-412Google Scholar]. Anthropometric studies by Birdsell [2Birdsell J.B. Microevolutionary Patterns in Aboriginal Australia. Oxford University Press, Oxford1993Google Scholar] led to his suggestion that a migratory wave into Australia included populations with affinities to tribal Indians. Genetic evidence for an Indian contribution to the Australian gene pool is contradictory; most studies of autosomal markers have not supported this hypothesis ([3Kirk R.L. Thorne A.G. The Origin of the Australians. Humanities Press, New Jersey1976Google Scholar, 4Nei M. Roychoudhury A.K. Evolutionary relationships of human populations on a global scale.Mol. Biol. Evol. 1993; 10: 927-943PubMed Google Scholar, 5Cavalli-Sforza L.L. Menozzi P. Piazza A. The History and Geography of Human Genes. Princeton University Press, Princeton1994Google Scholar]; [6Redd A.J. Stoneking M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations.Am. J. Hum. Genet. 1999; 65: 808-828Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar] and references therein). On the other hand, affinities between Australian Aboriginal People and southern Indians were suggested based on maternally inherited mitochondrial DNA [6Redd A.J. Stoneking M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations.Am. J. Hum. Genet. 1999; 65: 808-828Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar]. Here, we show additional DNA evidence in support of Huxley's hypothesis of an Indian-Australian connection using single-nucleotide polymorphisms (SNPs) and short tandem repeats (STRs) on the nonrecombining portion of the Y chromosome (NRY). Phylogenetic analyses of STR variation associated with a major Australian SNP lineage indicated tight clustering with southern Indian/Sri Lankan Y chromosomes. Estimates of the divergence time for these Indian and Australian chromosomes overlap with important changes in the archaeological and linguistic records in Australia. These results provide strong evidence for an influx of Y chromosomes from the Indian subcontinent to Australia that may have occurred during the Holocene. Approximately 50% [7Karafet T.M. Zegura S.L. Posukh O. Osipova L. Bergen A. Long J. Goldman D. Klitz W. Harihara S. de Knijff P. et al.Ancestral Asian source(s) of new world Y-chromosome founder haplotypes.Am. J. Hum. Genet. 1999; 64: 817-831Abstract Full Text Full Text PDF PubMed Scopus (234) Google Scholar, 8Kayser M. Brauer S. Weiss G. Schiefenhovel W. Underhill P.A. Stoneking M. Independent histories of human Y chromosomes from Melanesia and Australia.Am. J. Hum. Genet. 2001; 68: 173-190Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar] of the Y chromosomes in aboriginal Australians have a C → T transition [9Bergen A.W. Wang C.-Y. Tsai J. Jefferson K. Dey C. Smith K.D. Park S.C. Tsai S.J. Goldman D. An Asian-Native American paternal lineage identified by RPS4Y resequencing and by microsatellite haplotyping.Ann. Hum. Genet. 1999; 63: 63-80Crossref PubMed Google Scholar] at position 711 in the RPS4Y gene (RPS4Y711 C → T). This transition at RPS4Y (as well as a phylogenetically equivalent mutation: M216) defines haplogroup C (Hg C), one of five major haplogroups that form the base of a highly resolved evolutionary tree of NRY lineages [10Shen P. Wang F. Underhill P.A. Franco C. Yang W.H. Roxas A. Sung R. Lin A.A. Hyman R.W. Vollrath D. et al.Population genetic implications from sequence variation in four Y chromosome genes.Proc. Natl. Acad. Sci. USA. 2000; 97: 7354-7359Crossref PubMed Scopus (144) Google Scholar, 11Underhill P.A. Shen P. Lin A.A. Jin L. Passarino G. Yang W.H. Kauffman E. Bonne-Tamir B. Bertranpetit J. Francalacci P. et al.Y chromosome sequence variation and the history of human populations.Nat. Genet. 2000; 26: 358-361Crossref PubMed Scopus (742) Google Scholar, 12Hammer M.F. Karafet T.M. Redd A.J. Jarjanazi H. Santachiara-Benerecetti S. Soodyall H. Zegura S.L. Hierarchical patterns of global human Y-chromosome diversity.Mol. Biol. Evol. 2001; 18: 1189-1203Crossref PubMed Scopus (206) Google Scholar, 13YCC (The Y Chromosome Consortium). (2002). A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12, 339–348.Google Scholar]. Figure 1 shows an abbreviated form of this tree. Hg C chromosomes are found at varying frequencies in Asian, Native American, and Pacific populations; however, they are absent or at low frequency in Europe and Africa [7Karafet T.M. Zegura S.L. Posukh O. Osipova L. Bergen A. Long J. Goldman D. Klitz W. Harihara S. de Knijff P. et al.Ancestral Asian source(s) of new world Y-chromosome founder haplotypes.Am. J. Hum. Genet. 1999; 64: 817-831Abstract Full Text Full Text PDF PubMed Scopus (234) Google Scholar, 10Shen P. Wang F. Underhill P.A. Franco C. Yang W.H. Roxas A. Sung R. Lin A.A. Hyman R.W. Vollrath D. et al.Population genetic implications from sequence variation in four Y chromosome genes.Proc. Natl. Acad. Sci. USA. 2000; 97: 7354-7359Crossref PubMed Scopus (144) Google Scholar, 12Hammer M.F. Karafet T.M. Redd A.J. Jarjanazi H. Santachiara-Benerecetti S. Soodyall H. Zegura S.L. Hierarchical patterns of global human Y-chromosome diversity.Mol. Biol. Evol. 2001; 18: 1189-1203Crossref PubMed Scopus (206) Google Scholar]. In Australia, Hg C chromosomes have been found to be associated with a 16-bp deletion at the DYS390 STR locus (DYS390.1) [14Forster P. Kayser M. Meyer E. Roewer L. Pfeiffer H. Benkmann H. Brinkmann B. Phylogenetic resolution of complex mutational features at Y-STR DYS390 in aboriginal Australians and Papuans.Mol. Biol. Evol. 1998; 15: 1108-1114Crossref PubMed Scopus (49) Google Scholar], creating short alleles with 18–20 repeats. Chromosomes carrying short DYS390 alleles were found in 110 of 220 individuals sampled from Arnhem Land, the Northern Territories, the Kimberleys, and the Great Sandy Desert [8Kayser M. Brauer S. Weiss G. Schiefenhovel W. Underhill P.A. Stoneking M. Independent histories of human Y chromosomes from Melanesia and Australia.Am. J. Hum. Genet. 2001; 68: 173-190Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar, 14Forster P. Kayser M. Meyer E. Roewer L. Pfeiffer H. Benkmann H. Brinkmann B. Phylogenetic resolution of complex mutational features at Y-STR DYS390 in aboriginal Australians and Papuans.Mol. Biol. Evol. 1998; 15: 1108-1114Crossref PubMed Scopus (49) Google Scholar, 15Vandenberg N. van Oorschot R.A. Tyler-Smith C. Mitchell R.J. Y-chromosome-specific microsatellite variation in Australian aboriginals.Hum. Biol. 1999; 71: 915-931PubMed Google Scholar]. To investigate the origins of aboriginal Australian Hg C chromosomes, we expanded our previous SNP surveys [7Karafet T.M. Zegura S.L. Posukh O. Osipova L. Bergen A. Long J. Goldman D. Klitz W. Harihara S. de Knijff P. et al.Ancestral Asian source(s) of new world Y-chromosome founder haplotypes.Am. J. Hum. Genet. 1999; 64: 817-831Abstract Full Text Full Text PDF PubMed Scopus (234) Google Scholar, 12Hammer M.F. Karafet T.M. Redd A.J. Jarjanazi H. Santachiara-Benerecetti S. Soodyall H. Zegura S.L. Hierarchical patterns of global human Y-chromosome diversity.Mol. Biol. Evol. 2001; 18: 1189-1203Crossref PubMed Scopus (206) Google Scholar] by genotyping RPS4Y711 C → T in a total of 3,656 individuals from 52 worldwide populations (Figure 2), including the Warlpiri tribe from central Australia [16Roberts-Thomson J. Martinson J.J. Norwich J.T. Harding R.M. Clegg J.B. Boettcher B. An ancient common origin of aboriginal Australians and New Guinea highlanders is supported by alpha-globin haplotype analysis.Am. J. Hum. Genet. 1996; 58: 1017-1024PubMed Google Scholar], and 592 Y chromosomes from several localities in southern India [17Bamshad M. Kivisild T. Watkins W.S. Dixon M.E. Ricker C.E. Rao B.B. Naidu J.M. Prasad B.V. Reddy P.G. Rasanayagam A. et al.Genetic evidence on the origins of Indian caste populations.Genome Res. 2001; 11: 994-1004Crossref PubMed Scopus (271) Google Scholar] and Sri Lanka (hereafter defined as the Indian subcontinent). We found 433 Hg C chromosomes in 30 populations (Figure 2). To further differentiate Hg C chromosomes, we genotyped four SNPs associated with the RPS4Y711 T allele: M216, M217, M38, and M8 [10Shen P. Wang F. Underhill P.A. Franco C. Yang W.H. Roxas A. Sung R. Lin A.A. Hyman R.W. Vollrath D. et al.Population genetic implications from sequence variation in four Y chromosome genes.Proc. Natl. Acad. Sci. USA. 2000; 97: 7354-7359Crossref PubMed Scopus (144) Google Scholar, 11Underhill P.A. Shen P. Lin A.A. Jin L. Passarino G. Yang W.H. Kauffman E. Bonne-Tamir B. Bertranpetit J. Francalacci P. et al.Y chromosome sequence variation and the history of human populations.Nat. Genet. 2000; 26: 358-361Crossref PubMed Scopus (742) Google Scholar]. Figure 1 depicts the evolutionary relationships of Hg C and its subtypes: haplogroups C1, C2, and C3. Chromosomes that have the ancestral state at the M217, M38, and M8 mutational sites, and the derived state at both RPS4Y711 and M216, are designated "C*". The asterisk represents an interior node on the tree [13YCC (The Y Chromosome Consortium). (2002). A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12, 339–348.Google Scholar]. Approximately 20% of the Hg C chromosomes in our survey were C*. While C* chromosomes were present in combination with C3 chromosomes in mainland southeast Asia, and with C2 chromosomes in east Indonesia, coastal Papua New Guinea (PNG), and Micronesia, C* chromosomes were the only Hg C chromosomes present in our Indian subcontinent and aboriginal Australian samples (Figure 2). All other populations lacked C* chromosomes. Does this sharing of C* chromosomes support Huxley's hypothesis [1Huxley T.H. On the geographical distribution of the chief modifications of mankind.Ethnol. Soc. J. (Lond.). 1870; 2: 404-412Google Scholar] of an Indian-Australian connection? One complicating factor is the possibility that C* chromosomes are actually a heterogeneous mixture of derived haplogroups that are distinct in Indian subcontinent and Australian populations (i.e., marked by derived states at different SNPs yet to be discovered). To directly examine the evolutionary origins of C* chromosomes, we genotyped 10 Y-linked STRs in a sample of 63 C* chromosomes and 64 C1, C2, and C3 chromosomes. Figure 3 shows a median-joining (MJ) network [18Bandelt H.J. Forster P. Rohl A. Median joining networks for inferring intraspecific phylogenies.Mol. Biol. Evol. 1999; 16: 37-48Crossref PubMed Scopus (7761) Google Scholar] constructed from SNP and STR variation associated with these chromosomes. The MJ network rooted among C* chromosomes from the Indian subcontinent. The Indian subcontinent C* chromosomes were widely distributed across the central portion of the network, while the aboriginal Australian chromosomes formed a tight cluster that was closely affiliated with a subset of Indian subcontinent chromosomes. The single aboriginal Australian (Warlpiri) Y chromosome that was not part of the tight central cluster lacked the 16-bp deletion at DYS390.1, as did all other Hg C chromosomes (including C* chromosomes from the Indian subcontinent). The DYS390.1 deletion is very common in Australia, and it appears to be Australian specific. Similar network clusters were obtained when SNPs were excluded from the phylogenetic analysis (data not shown). Measures of average mutational divergence within and between populations of Hg C chromosomes (Table 1) are consistent with the aforementioned phylogenetic inferences. First, Indian subcontinent chromosomes are more diverse than aboriginal Australian chromosomes. Second, the average number of mutational steps between Indian subcontinent and aboriginal Australian Hg C chromosomes (6.88) is less than the number of mutational steps within those from the Indian subcontinent (7.32). Finally, the lowest average number of pairwise differences among haplotypes (6.88) in Table 1 is between aboriginal Australian and Indian subcontinent haplotypes rather than between aboriginal Australian chromosomes and those of their close geographic neighbors in Melanesia.Table 1Haplogroup C STR Diversity within and between Population RegionsSampleAAPISCSEAEINMELPOLAboriginal Australian People (AAP)4.106.889.339.478.948.99Indian subcontinent (ISC)0.2567.328.8911.4510.7610.11Southeast Asians (SEA)0.4590.1077.1211.9812.3413.75East Indonesians (EIN)0.6531.2651.2949.8211.7113.10Melanesians (MEL)0.5010.8081.0560.8089.479.31Polynesians (POL)0.8860.7691.2771.7780.3933.34The average number of pairwise differences are shown within (PiX along diagonal) and between populations (PiXY above diagonal); pairwise (δμ)2 genetic distance values are shown below the diagonal. Values were computed using ARLEQUIN 33Schneider S. Kueffer J.-M. Roessli D. Excoffier L. ARLEQUIN: A Software for Population Genetic Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva1998Google Scholar and MICROSAT 34Minch, E., Ruiz-Linares, A., Goldstein, D., Feldman, M.W., and Cavalli-Sforza, L.L. (1997). MICROSAT v.1.5d: A Computer Program for Calculating Various Statistics on Microsatellite Allele Data. Stanford, CA: Department of Genetics, Stanford University).Google Scholar.AAP = 14 Central Desert, 5 Great Sandy Desert, and 2 Western Australians; ISC = 16 Southern Indians and 3 Sri Lankans; SEA = 12 Yao, 11 Tuja, 3 Miao, 3 Vietnamese, and 1 Malay; EIN = 10 Moluccans, 8 Nusa Tengarrans, and 1 Javan; MEL = 10 Vanuatuans and 5 Papua New Guineans; and POL = 13 Samoans, 8 Tahitians, and 3 Tongans. Open table in a new tab The average number of pairwise differences are shown within (PiX along diagonal) and between populations (PiXY above diagonal); pairwise (δμ)2 genetic distance values are shown below the diagonal. Values were computed using ARLEQUIN 33Schneider S. Kueffer J.-M. Roessli D. Excoffier L. ARLEQUIN: A Software for Population Genetic Analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva1998Google Scholar and MICROSAT 34Minch, E., Ruiz-Linares, A., Goldstein, D., Feldman, M.W., and Cavalli-Sforza, L.L. (1997). MICROSAT v.1.5d: A Computer Program for Calculating Various Statistics on Microsatellite Allele Data. Stanford, CA: Department of Genetics, Stanford University).Google Scholar. AAP = 14 Central Desert, 5 Great Sandy Desert, and 2 Western Australians; ISC = 16 Southern Indians and 3 Sri Lankans; SEA = 12 Yao, 11 Tuja, 3 Miao, 3 Vietnamese, and 1 Malay; EIN = 10 Moluccans, 8 Nusa Tengarrans, and 1 Javan; MEL = 10 Vanuatuans and 5 Papua New Guineans; and POL = 13 Samoans, 8 Tahitians, and 3 Tongans. If we are, indeed, detecting a genetic connection in accord with Huxley's hypothesis, it would be interesting to estimate the timing of divergence between Australian and Indian C* chromosomes. To explore this further, we used the STR data to estimate divergence times using two published methods. In both methods, we assumed a generation time of 25 years. Furthermore, we assumed a mutation rate of 2.08 × 10−3 that is based on the average rate from three pedigree studies [19Heyer E. Puymirat J. Dieltjes P. Bakker E. de Knijff P. Estimating Y chromosome specific microsatellite mutation frequencies using deep rooting pedigrees.Hum. Mol. Genet. 1997; 6: 799-803Crossref PubMed Scopus (224) Google Scholar, 20Bianchi N.O. Catanesi C.I. Bailliet G. Martinez-Marignac V.L. Bravi C.M. Vidal-Rioja L.B. Herrera R.J. Lopez-Camelo J.S. Characterization of ancestral and derived Y-chromosome haplotypes of New World native populations.Am. J. Hum. Genet. 1998; 63: 1862-1871Abstract Full Text Full Text PDF PubMed Scopus (136) Google Scholar, 21Kayser M. Roewer L. Hedman M. Henke L. Henke J. Brauer S. Kruger C. Krawczak M. Nagy M. Dobosz T. Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in Father/Son pairs.Am. J. Hum. Genet. 2000; 66: 1580-1588Abstract Full Text Full Text PDF PubMed Scopus (303) Google Scholar] and included 8,169 meioses in 9 Y-STR loci. In the first dating method, the (δμ)2 genetic distance was selected because it provides a robust divergence estimate that retains linearity with increasing time and it is largely independent of population size [22Goldstein D.B. Ruiz Linares A. Cavalli-Sforza L.L. Feldman M.W. Genetic absolute dating based on microsatellites and the origin of modern humans.Proc. Natl. Acad. Sci. USA. 1995; 92: 6723-6727Crossref PubMed Scopus (641) Google Scholar]. To calculate 95% CIs, 1,000 bootstrap samples were performed to obtain the standard errors of (δμ)2. The average (δμ)2 divergence between Indian and Australian C* chromosomes was 0.256 ± 0.105. Thus, the age of the divergence is 62 generations (95% CI = 12–111 generations) ((δμ)2 = 2 μt, where μ is the mutation rate, and t is the generation time) or 1,550 years (95% CI = 300–2,775 years). The variance displayed in these 95% CIs does not include the uncertainty in the mutation rate. Second, we used a Bayesian method for estimating the time to the most recent common ancestor (TMRCA) described in Walsh [23Walsh B. Estimating the time to the most recent common ancestor for the Y chromosome or mitochondrial DNA for a pair of individuals.Genetics. 2001; 158: 897-912PubMed Google Scholar]. We used this method to calculate 95% CIs for the TMRCA using tallies of the number of STR differences between two chromosomes; in this case, the modal C* haplotype from India and the modal C* haplotype from Australia. The TMRCA is equivalent to the divergence time between these two modal haplotypes. The resulting posterior distribution for the TMRCA (i.e., the divergence time in this example) between Indian and Australian C* chromosomes had a mean of 195 generations (95% CI = 49–532 generations) or 4,875 years (95% CI = 1,255–13,300 years). The Bayesian analysis [23Walsh B. Estimating the time to the most recent common ancestor for the Y chromosome or mitochondrial DNA for a pair of individuals.Genetics. 2001; 158: 897-912PubMed Google Scholar] requires an estimate of the effective population size, Ne, to generate a prior distribution. While we assumed Ne = 5,000, larger effective population sizes produced nearly identical results. This is a conservative value, as assuming smaller values of Ne decreases the divergence. The precision of the estimated divergence times should be considered somewhat cautiously because there are uncertainties with regard to STR mutation rates and processes. We stress, however, that we selected the slowest mutation rate value that still seems reasonable, which errs on the side of overestimating the TMRCA. Nevertheless, both dating methods (i.e., Bayesian and (δμ)2) yielded times that are consistent with a relatively recent (e.g., Holocene) divergence between these populations of chromosomes, as expected from the low number of pairwise differences in STR allele lengths seen in Table 1. Furthermore, the patterns of divergence are consistent with more recent C* affinities between Australia and the Indian subcontinent than between Australia and Melanesia. The combined genetic distance, phylogenetic, and dating analyses provide evidence for recent shared ancestry of some aboriginal Australian and Indian subcontinent C* chromosomes. Moreover, the fact that aboriginal Australian chromosomes represent a subset of the C* diversity found in the Indian subcontinent may provide evidence that the Australian C* chromosomes descended from an Indian subcontinent ancestor(s). Indeed, the positions of Indian subcontinent C* lineages in Figure 3 (i.e., basal to many of the derived haplotypes) lends support to the hypothesis of an Indian origin of the RPS4Y711 C → T mutation. The presence of the DYS390.1 deletion on all but one Australian C* chromosome in this survey is suggestive of a strong bottleneck associated with the spread of C* chromosomes to or within Australia. The absence of the DYS390.1 deletion in the Indian subcontinent sample may imply that the deletion event occurred either in India, on a Y chromosome that was migrating from India to Australia, or in Australia well after the migration of C* chromosomes from India. Further studies are needed to distinguish among these hypotheses and to infer the evolutionary forces that resulted in such high frequencies of C* chromosomes carrying the DYS390.1 deletion in contemporary populations of Australian Aboriginal People. In sum, we found that 50% of the Y chromosomes sampled from aboriginal Australians share common ancestry with a set of Y chromosomes that represent less than 2% of the sampled Indian subcontinent paternal gene pool. The similarity among C* chromosomes is unlikely to have been caused by chance convergence because we genotyped ten independent STRs. The observed pattern is not specific to central Australians, since our sample also included individuals from the Great Sandy Desert and from Western Australia, and our estimate of the frequency of C* chromosomes agrees remarkably well with other studies of greater numbers of aboriginal Australian Y chromosomes in Arnhem Land, the Great Sandy Desert, the Kimberleys, and the Northern Territory [8Kayser M. Brauer S. Weiss G. Schiefenhovel W. Underhill P.A. Stoneking M. Independent histories of human Y chromosomes from Melanesia and Australia.Am. J. Hum. Genet. 2001; 68: 173-190Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar, 14Forster P. Kayser M. Meyer E. Roewer L. Pfeiffer H. Benkmann H. Brinkmann B. Phylogenetic resolution of complex mutational features at Y-STR DYS390 in aboriginal Australians and Papuans.Mol. Biol. Evol. 1998; 15: 1108-1114Crossref PubMed Scopus (49) Google Scholar, 15Vandenberg N. van Oorschot R.A. Tyler-Smith C. Mitchell R.J. Y-chromosome-specific microsatellite variation in Australian aboriginals.Hum. Biol. 1999; 71: 915-931PubMed Google Scholar]. A southern route of migration from Africa to Australia in the Pleistocene has often been suggested to explain similarities among some populations in Africa, India, Southeast Asia, and Australia [4Nei M. Roychoudhury A.K. Evolutionary relationships of human populations on a global scale.Mol. Biol. Evol. 1993; 10: 927-943PubMed Google Scholar, 5Cavalli-Sforza L.L. Menozzi P. Piazza A. The History and Geography of Human Genes. Princeton University Press, Princeton1994Google Scholar]. The presence of closely related C* chromosomes in populations sampled from the tropical corridor between south Asia and the Pacific is consistent with this hypothesis (Figure 2). However, our analyses suggest a mid-Holocene common ancestry of aboriginal Australian and Indian subcontinent C* chromosomes. The divergence times reported here correspond with a series of changes in the Australian anthropological record between 5,000 years ago and 3,000 years ago, including the introduction of the dingo [24Gollan K. Prehistoric dogs in Australia: an Indian origin?.in: Misra V.N. Bellwood P. Recent Advances in Indo-Pacific Prehistory. Oxford and IBH, New Dehli1985: 439-443Google Scholar]; the spread of the Australian Small Tool tradition [25Glover I.C. Presland G. Microliths in Indonesian flaked stone industries.in: Misra V.N. Bellwood P. Recent Advances in Indo-Pacific Prehistory. Oxford and IBH, New Dehli1985: 185-195Google Scholar]; the appearance of plant-processing technologies, especially complex detoxification of cycads [26Beaton, J. (1977). Dangerous harvest: investigations in the late prehistoric occupation of upland south-east central Queensland. PhD thesis, Australian National University, Canberra, Australia.Google Scholar]; and the expansion of the Pama-Nyungan language over seven-eighths of Australia [27Evans N. Jones R. The cradle of the Pama-Nyungans: archaeological and linguistic speculations.in: McConvell P. Evans N. Archaeology and Linguistics: Aboriginal Australia in Global Perspective. Oxford University Press, Oxford1997: 385-417Google Scholar]. Although there is no consensus among anthropologists, the former three changes may have links to India, perhaps the most relevant of which is the introduction of the dingo, whose ocean transit was almost certainly on board a boat. In addition, Dixon [28Dixon R.M.W. The Languages of Australia. Cambridge University Press, New York1980Google Scholar] noted some similarities between Dravidian languages of southern India and Pama-Nyungan languages of Australia. The combined genetic (Y chromosome and mitochondrial DNA [6Redd A.J. Stoneking M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations.Am. J. Hum. Genet. 1999; 65: 808-828Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar]) and anthropological evidence supports Holocene contact between the Indian subcontinent and Australia, although there is a need for more research in this area. Genetic dating of the divergence between Australian and Indian C* chromosomes will improve as the number of loci typed increases [23Walsh B. Estimating the time to the most recent common ancestor for the Y chromosome or mitochondrial DNA for a pair of individuals.Genetics. 2001; 158: 897-912PubMed Google Scholar], as locus/allele-specific mutation rates are refined [29Capelli C. Wilson J.F. Richards M. Stumpf M.P. Gratrix F. Oppenheimer S. Underhill P. Pascali V.L. Ko T.M. Goldstein D.B. A predominantly indigenous paternal heritage for the Austronesian-speaking peoples of insular Southeast Asia and Oceania.Am. J. Hum. Genet. 2001; 68: 432-443Abstract Full Text Full Text PDF PubMed Scopus (112) Google Scholar], and as simulation methods are developed that consider the effects of including only subsets of chromosomes sampled in different populations [30Stumpf M.P.H. Goldstein D.B. Genealogical and evolutionary inference with the human Y chromosome.Science. 2001; 291: 1738-1742Crossref PubMed Scopus (67) Google Scholar]. It is important to emphasize that Australian and Indian non-Hg C chromosomes did not show close affinities and that paternal variation cannot be used to infer the complete genetic history of Australian populations. On the other hand, weak signals for population relationships based on autosomal data may be magnified on the NRY as a result of its lack of recombination and susceptibility to higher levels of genetic drift. Therefore, the NRY can be an important tool for reconstructing the history of human populations. We thank the Warlpiri tribe from central Australia and others who donated DNA samples. We also thank Ian Wilson, Stephen Zegura, and David Meltzer for helpful comments. This publication was made possible by grant GM-53566 from the National Institute of General Medical Sciences and by grant OPP-9806759 from the National Science Foundation (NSF) (to M.F.H.) and by National Institutes of Health (NIH) grant GM-59290 and NSF grant SBR-9818215 to L.B.J. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH or NSF.
Referência(s)