Taiwan Y-chromosomal DNA variation and its relationship with Island Southeast Asia

BMC Genetics

Marie Lin²  Chun-Lin He²  Chien-Liang Lee²  Jun-Hun Loo²  Ying-Hui Lai²  Ju-Chen Yen²  Estella S Poloni¹  Jean A Trejaut² 

[1] Laboratory of Anthropology, Genetics and Peopling History, Anthropology Unit, Department of Genetics and Evolution, University of Geneva, Geneva, Switzerland;Mackay Memorial Hospital, Taipei, Molecular Anthropology Laboratory, 45 Min-Sheng Road,225115 Tamsui, New Taipei city, Taiwan

关键词: Haplogroup O1a;    Island Southeast Asia;    Taiwan;    Austronesian migration;    Y-SNP;    Y-STR;    Y chromosome;   

Others  :  866406
DOI  :  10.1186/1471-2156-15-77

 received in 2013-10-25, accepted in 2014-06-10,  发布年份 2014

【 摘 要 】

Background

Much of the data resolution of the haploid non-recombining Y chromosome (NRY) haplogroup O in East Asia are still rudimentary and could be an explanatory factor for current debates on the settlement history of Island Southeast Asia (ISEA). Here, 81 slowly evolving markers (mostly SNPs) and 17 Y-chromosomal short tandem repeats were used to achieve higher level molecular resolution. Our aim is to investigate if the distribution of NRY DNA variation in Taiwan and ISEA is consistent with a single pre-Neolithic expansion scenario from Southeast China to all ISEA, or if it better fits an expansion model from Taiwan (the OOT model), or whether a more complex history of settlement and dispersals throughout ISEA should be envisioned.

Results

We examined DNA samples from 1658 individuals from Vietnam, Thailand, Fujian, Taiwan (Han, plain tribes and 14 indigenous groups), the Philippines and Indonesia. While haplogroups O1a*-M119, O1a1*-P203, O1a2-M50 and O3a2-P201 follow a decreasing cline from Taiwan towards Western Indonesia, O2a1-M95/M88, O3a*-M324, O3a1c-IMS-JST002611 and O3a2c1a-M133 decline northward from Western Indonesia towards Taiwan. Compared to the Taiwan plain tribe minority groups the Taiwanese Austronesian speaking groups show little genetic paternal contribution from Han. They are also characterized by low Y-chromosome diversity, thus testifying for fast drift in these populations. However, in contrast to data provided from other regions of the genome, Y-chromosome gene diversity in Taiwan mountain tribes significantly increases from North to South.

Conclusion

The geographic distribution and the diversity accumulated in the O1a*-M119, O1a1*-P203, O1a2-M50 and O3a2-P201 haplogroups on one hand, and in the O2a1-M95/M88, O3a*-M324, O3a1c-IMS-JST002611 and O3a2c1a-M133 haplogroups on the other, support a pincer model of dispersals and gene flow from the mainland to the islands which likely started during the late upper Paleolithic, 18,000 to 15,000 years ago. The branches of the pincer contributed separately to the paternal gene pool of the Philippines and conjointly to the gene pools of Madagascar and the Solomon Islands. The North to South increase in diversity found for Taiwanese Austronesian speaking groups contrasts with observations based on mitochondrial DNA, thus hinting to a differentiated demographic history of men and women in these populations.

【 授权许可】

   
2014 Trejaut et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Chiung WVT: Language attitudes toward written Taiwanese. J Multiling Multicult Devel 2001, 22:502-523.
• [2]Murdock GP: Genetic classification of the austronesian languages: a key to oceanic culture history. Ethnology 1964, 3:117-126.
• [3]Blust R: The prehistory of the Austronesian-speaking peoples: the view from language. J World Prehistory 1995, 9:453-510.
• [4]Bellwood P: Prehistory of the Indo-Malaysian Archipelago. Honolulu: HI: University of Hawaii Press; 1997.
• [5]Diamond J, Bellwood P: Farmers and their languages: the first expansions. Science 2003, 300:597-603.
• [6]Underhill PA, Kivisild T: Use of Y chromosome and mitochondrial DNA. Population structure in tracing human migrations. Annu Rev Genet 2007, 41:539-564.
• [7]Delfin F, Salvador JM, Calacal GC, Perdigon HB, Tabbada KA, Villamor LP, Halos SC, Gunnarsdottir E, Myles S, Hughes DA, Xu S, Jin L, Lao O, Kayser M, Hurles ME, Stoneking M, De Ungria MC: The Y-chromosome landscape of the Philippines: extensive heterogeneity and varying genetic affinities of Negrito and non-Negrito groups. Eur J Hum Genet 2010, 19:224-230.
• [8]Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, Hammer MF: New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res 2008, 18:830-838.
• [9]Su B, Jin L, Underhill P, Martinson J, Saha N, McGarvey ST, Shriver MD, Chu J, Oefner P, Chakraborty R, Deka R: Polynesian origins: insights from the Y chromosome. Proc Natl Acad Sci U S A 2000, 97:8225-8228.
• [10]Friedlaender JS, Friedlaender FR, Reed FA, Kidd KK, Kidd JR, Chambers GK, Lea RA, Loo JH, Koki G, Hodgson JA, Merriwether DA, Weber JL: The genetic structure of Pacific Islanders. PLoS Genet 2008, 4(1):e19.
• [11]Cai X, Qin Z, Wen B, Xu S, Wang Y, Lu Y, Wei L, Wang C, Li S, Huang X, Jin L, Li H: Human migration through bottlenecks from Southeast Asia into East Asia during last glacial maximum revealed by Y chromosomes. PLoS One 2011, 6:e24282.
• [12]Kim SH, Kim KC, Shin DJ, Jin HJ, Kwak KD, Han MS, Song JM, Kim W: High frequencies of Y-chromosome haplogroup O2b-SRY465 lineages in Korea: a genetic perspective on the peopling of Korea. Investig Genet 2011, 2:10.
• [13]Abbott WG, Winship IM, Gane EJ, Finau SA, Munn SR, Tukuitonga CE: Genetic diversity and linkage disequilibrium in the Polynesian population of Niue Island. Hum Biol 2006, 78:131-145.
• [14]Tumonggor MK, Karafet TM, Hallmark B, Lansing JS, Sudoyo H, Hammer MF, Cox MP: The Indonesian archipelago: an ancient genetic highway linking Asia and the Pacific. J Hum Genet 2013, 58:165-173.
• [15]Melton T, Clifford S, Martinson J, Batzer M, Stoneking M: Genetic evidence for the proto-Austronesian homeland in Asia: mtDNA and nuclear DNA variation in Taiwanese aboriginal tribes. Am J Hum Genet 1998, 63:1807-1823.
• [16]Hill C, Soares P, Mormina M, Macaulay V, Meehan W, Blackburn J, Clarke D, Raja JM, Ismail P, Bulbeck D, Oppenheimer S, Richards M: Phylogeography and ethnogenesis of aboriginal southeast asians. Mol Biol Evol 2006, 23:2480-2491.
• [17]Soares P, Trejaut JA, Loo J-H, Hill C, Mormina M, Lee CL, Chen YM, Hudjashov G, Forster P, Macaulay V, Bulbeck D, Oppenheimer S, Lin M, Richards MB: Climate change and postglacial human dispersals in southeast Asia. Mol Biol Evol 2008, 25:1209-1218.
• [18]Tabbada KA, Trejaut J, Loo JH, Chen YM, Lin M, Mirazon-Lahr M, Kivisild T, De Ungria MC: Philippine mitochondrial DNA diversity: a populated viaduct between Taiwan and Indonesia? Mol Biol Evol 2010, 27:21-31.
• [19]Trejaut JA, Kivisild T, Loo JH, Lee CL, He CL, Hsu CJ, Li ZY, Lin M: Traces of archaic mitochondrial lineages persist in Austronesian speaking Formosan populations. PLoS Biol 2005, 3:e247.
• [20]Sagart L: Sino-Tibetan-Austronesian: An Updated and Improved Argument. London: RoutledgeCurzon; 2004:161-176.
• [21]Richards M, Oppenheimer S, Sykes B: mtDNA suggests Polynesian origins in eastern Indonesia. Am J Hum Genet 1998, 63:1234-1236.
• [22]Cox MP: Indonesian mitochondrial DNA and its opposition to a Pleistocene Era origin of proto-Polynesians in Island Southeast Asia. Hum Biol 2005, 77(no. 2):179-188.
• [23]Oppenheimer S, Richards M: Fast trains, slow boats, and the ancestry of the Polynesian islanders. Sci Prog 2001, 84:157-181.
• [24]Bellwood P, Dizon E: The Batanes archaeological project and the ‘Out of Taiwan’ hypothesis for Austronesian dispersal. J Austronesian Studies (Taitung, Taiwan) 2005, 1:1-32.
• [25]Loo JH, Trejaut JA, Yen JC, Chen ZS, Lee CL, Lin M: Genetic affinities between the Yami tribe people of Orchid Island and the Philippine Islanders of the Batanes archipelago. BMC Genet 2011, 12:21.
• [26]Karafet TM, Hallmark B, Cox MP, Sudoyo H, Downey S, Lansing JS, Hammer MF: Major east–west division underlies Y chromosome stratification across Indonesia. Mol Biol Evol 2010, 27:1833-1844.
• [27]Li H, Wen B, Chen SJ, Su B, Pramoonjago P, Liu Y, Pan S, Qin Z, Liu W, Cheng X, Yang N, Li X, Tran D, Lu D, Hsu MT, Deka R, Marzuki S, Tan CC, Jin L: Paternal genetic affinity between Western Austronesians and Daic populations. BMC Evol Biol 2008, 8:146.
• [28]Jin L, Su B: Natives or immigrants: modern human origin in East Asia. Nat Rev Genet 2000, 1:126-133.
• [29]Shi H, Dong Y, Wen B, C-J X i, Chakraborty R, Jin L, Su B: Y -chromosome evidence of Southern origin of the East Asian–specific H aplogroup O3 -M 1 2 2. Am J Hum Genet 2005, 77:408-419.
• [30]Xue Y, Zerjal T, Bao W, Zhu S, Shu Q, Xu J, Du R, Fu S, Li P, Hurles ME, Yang H, Tyler-Smith C: Male demography in East Asia: a north–south contrast in human population expansion times. Genetics 2006, 172(4):2431-2439.
• [31]Zhang F, Su B, Zhang Y-P, Jin L: Genetic studies of human diversity in East Asia. Philos Trans R Soc Lond B Biol Sci 2007, 362(1482):987-995.
• [32]Hwa HL, Tseng LH, Ko TM, Chang YY, Yin HY, Su YN, Lee JC: Seventeen Y-chromosomal short tandem repeat haplotypes in seven groups of population living in Taiwan. Int J Legal Med 2010, 124:295-300.
• [33]Wu F-C, Chen M-Y, Chao C-H, Pu C-E: Study on the genetic polymorphisms of Y chromosomal DNA short tandem repeat loci applied to analyzing the relative affinities among ethnic groups in Taiwan. Forensic Sci Int Genet Suppl Ser 2013, 4:e69-e70.
• [34]Tsai LC, Yuen TY, Hsieh HM, Lin M, Tzeng CH, Huang NE, Linacre A, Lee JC: Haplotype frequencies of nine Y-chromosome STR loci in the Taiwanese Han population. Int J Legal Med 2002, 116:179-183.
• [35]Avarez I, Royo LJ, Fernandez I, Gutierrez JP, Gomez E, Goyache F: Genetic relationships and admixture among sheep breeds from Northern Spain assessed using microsatellites. J Anim Sci 2004, 82:2246-2252.
• [36]Lewis MP: Ethnologue: Languages of the World, vol. Sixteenth Edition. Dallas, Texas USA: SIL International Publications; 2009. 7500 West Camp Wisdom Road. Online version: http://www.ethnologue.com/ webcite; 2009000000
• [37]Li D, Li H, Ou C, Lu Y, Sun Y, Yang B, Qin Z, Zhou Z, Li S, Jin L: Paternal genetic structure of Hainan aborigines isolated at the entrance to East Asia. PLoS One 2008, 3:e2168.
• [38]Tan S, Yang M, Yu H, Dong Y, Shou W, Zou J, Tang W, Guo Y, Xiao C: Y-chromosome polymorphisms define the origin of the Mang, an isolated population in China. Ann Hum Biol 2007, 34:573-581.
• [39]Brucato N, Mazieres S, Guitard E, Giscard PH, Bois E, Larrouy G, Dugoujon JM: The Hmong Diaspora: preserved South-East Asian genetic ancestry in French Guianese Asians. C R Biol 2012, 335:698-707.
• [40]Karafet TM, Lansing JS, Redd AJ, Reznikova S, Watkins JC, Surata SP, Arthawiguna WA, Mayer L, Bamshad M, Jorde LB, Hammer MF: Balinese Y-chromosome perspective on the peopling of Indonesia: genetic contributions from pre-neolithic hunter-gatherers, Austronesian farmers, and Indian traders. Hum Biol 2005, 77:93-114.
• [41]Wen B, Li H, Lu D, Song X, Zhang F, He Y, Li F, Gao Y, Mao X, Zhang L, Qian J, Tan J, Jin J, Huang W, Deka R, Su B, Chakraborty R, Jin L: Genetic evidence supports demic diffusion of Han culture. Nature 2004, 431:302-305.
• [42]Dulik MC, Osipova LP, Schurr TG: Y-chromosome variation in Altaian Kazakhs reveals a common paternal gene pool for Kazakhs and the influence of Mongolian expansions. PLoS One 2011, 6:e17548.
• [43]Yan S, Wang C-C, Li H, Li S-L, Jin L, Genographic Consortion: An updated tree of Y-chromosome Haplogroup O and revised phylogenetic positions of mutations P164 and PK4. Eur J Hum Genet 2011, 19(9):1013-1015.
• [44]YCC: Y Chromosome Consortium, A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 2002, 12:339-348.
• [45]ISOGG: Y-DNA Haplogroup Tree. International Society of Genetic Genealogy. 2009. Version: 4.06, Date: 10 February 2009; Available: http://www.isogg.org/tree/ webcite
• [46]Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, Kauffman E, Bonne-Tamir B, Bertranpetit J, Francalacci P, Ibrahim M, Jenkins T, Kidd JR, Mehdi SQ, Seielstad MT, Wells RS, Piazza A, Davis RW, Feldman MW, Cavalli-Sforza LL, Oefner PJ: Y chromosome sequence variation and the history of human populations. Nat Genet 2000, 26:358-361.
• [47]Qamar R, Ayub Q, Mohyuddin A, Helgason A, Mazhar K, Mansoor A, Zerjal T, Tyler-Smith C, Mehdi SQ: Y-chromosomal DNA variation in Pakistan. Am J Hum Genet 2002, 70:1107-1124.
• [48]Nei M: Molecular Evolutionary Genetics. New York: Columbia University Press; 1987.
• [49]Zhivotovsky LA: Estimating divergence time with the Use of microsatellite genetic distances: impacts of population growth and gene flow. Mol Biol Evol 2001, 18:700-709.
• [50]Zhivotovsky LA, Underhill PA, Cinnio?lu C, Kayser M, Morar B, Kivisild T, Scozzari R, Cruciani F, Destro-Bisol G, Spedini G, Chambers GK, Herrera RJ, Yong KK, Gresham D, Tournev I, Feldman MW, Kalaydjieva L: The effective mutation rate at Y chromosome short tandem repeats, with application to human population-divergence time. Am J Hum Genet 2004, 74:50-61.
• [51]Sengupta S, Zhivotovsky LA, King R, Mehdi SQ, Edmonds CA, Chow CE, Lin AA, Mitra M, Sil SK, Ramesh A, Usha Rani MV, Thakur CM, Cavalli-Sforza LL, Majumder PP, Underhill PA: 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 2006, 78:202-221.
• [52]Bertorelle G, Excoffier L: Inferring admixture proportions from molecular data. Mol Biol Evol 1998, 15:1298-1311.
• [53]Dupanloup I, Bertorelle G: Inferring admixture proportions from molecular data: extension to any number of parental populations. Mol Biol Evol 2001, 18(4):672-675.
• [54]Maca-Meyer N, Arnay M, Rando JC, Flores C, Gonzalez AM, Cabrera VM, Larruga JM: Ancient mtDNA analysis and the origin of the Guanches. Eur J Hum Genet 2004, 12:155-162.
• [55]Schneider S, Roessli D, Excoffier L: Arlequin Version 2.000: A Software for Population Genetics Data Analysis. Geneva: University of Geneva, Genetics and Biochemistry laboratory; 2000.
• [56]Addinsoft: XLSTAT Software Version 7.5.2. 2008 2008. http://www.xlstat.com/ webcite
• [57]Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
• [58]Delfin FC, Madrid BJ, Tan MP, De Ungria MC: Y-STR analysis for detection and objective confirmation of child sexual abuse. Int J Legal Med 2005, 119:158-163.
• [59]Dupuy B, Stenersen M, Egeland T, Olaisen B: Y-chromosomal microsatellite mutation rates: differences in mutation rate between and within loci. Hum Mutat 2004, 23:117-124.
• [60]Gusmao L, Sanchez-Diz P, Calafell F, Martin P, Alonso CA, Alvarez-Fernandez F, Alves C, Borjas-Fajardo L, Bozzo WR, Bravo ML, Builes JJ, Capilla J, Carvalho M, Castillo C, Catanesi CI, Corach D, Di Lonardo AM, Espinheira R, Fagundes De Carvalho E, Farfan MJ, Figueiredo HP, Gomes I, Lojo MM, Marino M, Pinheiro MF, Pontes ML, Prieto V, Ramos-Luis E, Riancho JA, Souza Goes AC: Mutation rates at Y chromosome specific microsatellites. Hum Mutat 2005, 26:520-528.
• [61]Kayser M, Brauer S, Weiss G, Underhill PA, Roewer L, Schiefenhovel W, Stoneking M: Melanesian origin of Polynesian Y chromosomes. Curr Biol 2000, 10:1237-1246.
• [62]Ko AM-S, Chen C-Y, Fu Q, Delfin F, Li M, Chiu H-L, Stoneking M, Ko Y-C: Early Austronesians: into and Out of Taiwan. Am J Hum Genet 2014, 94:426-436.
• [63]ISOGG: International Society of Genetic Genealogy (2012). Y-DNA Haplogroup Tree 2012. 2012. Version: 7.45 Date: 9 August 2012, http://www.isogg.org/tree/index.html webcite
• [64]Nonaka I, Minaguchi K, Takezaki N: Y-chromosomal binary haplogroups in the Japanese population and their relationship to 16 Y-STR polymorphisms. Ann Hum Genet 2007, 71:480-495.
• [65]van Oven M, Hammerle JM, van Schoor M, Kushnick G, Pennekamp P, Zega I, Lao O, Brown L, Kennerknecht I, Kayser M: Unexpected island effects at an extreme: reduced Y chromosome and mitochondrial DNA diversity in Nias. Mol Biol Evol 2011, 28:1349-1361.
• [66]Lansing JS, Cox MP, de Vet TA, Downey SS, Hallmark B, Sudoyo H: An ongoing Austronesian expansion in Island Southeast Asia. J Anthropol Archaeol 2011, 30:262-272.
• [67]Kayser M, Choi Y, van Oven M, Mona S, Brauer S, Trent RJ, Suarkia D, Schiefenhovel W, Stoneking M: The impact of the Austronesian expansion: evidence from mtDNA and Y chromosome diversity in the Admiralty Islands of Melanesia. Mol Biol Evol 2008, 25:1362-1374.
• [68]Tofanelli S, Bertoncini S, Castri L, Luiselli D, Calafell F, Donati G, Paoli G: On the origins and admixture of Malagasy: new evidence from high-resolution analyses of paternal and maternal lineages. Mol Biol Evol 2009, 26:2109-2124.
• [69]Mirabal S, Cadenas A, Garcia-Bertrand R, Herrera R: Ascertaining the role of Taiwan as a source for the Austronesian expansion. Am J Phys Anthropol 2013, 150:551-564.
• [70]Hammer MF, Karafet TM, Park H, Omoto K, Harihara S, Stoneking M, Horai S: Dual origins of the Japanese: common ground for hunter-gatherer and farmer Y chromosomes. J Hum Genet 2006, 51:47-58.
• [71]Jin HJ, Kwak KD, Hammer MF, Nakahori Y, Shinka T, Lee JW, Jin F, Jia X, Tyler-Smith C, Kim W: Y-chromosomal DNA haplogroups and their implications for the dual origins of the Koreans. Hum Genet 2003, 114:27-35.
• [72]Friedlaender JS, Friedlaender FR, Hodgson JA, Stoltz M, Koki G, Horvat G, Zhadanov S, Schurr TG, Merriwether DA: Melanesian mtDNA complexity. PLoS One 2007, 2(2):e248. wwwplosoneorg 2007:e248
• [73]Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW: Genetic structure of human populations. Science 2002, 298:2381-2385.
• [74]Sanchez-Mazas A, Fernandez-Viña M, Middleton D, Hollenbach JA, Buhler S, Di D, Rajalingam R, Dugoujon JM, Mack S, Thorsby E: Immunogenetics as a tool in anthropological studies. Immunology 2011, 133:143-164.
• [75]Sanchez-Mazas A, Osipova L, Dugoujon JM, Sagart L, Poloni ES: The GM genetic polymorphism in Taiwan aborigines: new data revealing remarkable differentiation patterns. In Past Human Migrations in East Asia: Matching Archaeology, Linguistics and Genetics. Edited by Sanchez-Mazas A, Blench R, Ross M, Peiros I, Lin M. London, New York: Routledge; 2008:313-333.
• [76]Park MJ, Lee HY, Yang WI, Shin KJ: Understanding the Y chromosome variation in Korea–relevance of combined haplogroup and haplotype analyses. Int J Legal Med 2012, 126:589-599.
• [77]Wang C-C, Yan S, Qin Z-D, Lu Y, Ding Q-L, Wei L-H, Li S-L, Yang Y-J, Jin L, Li H: Late Neolithic expansion of ancient Chinese revealed by Y chromosome haplogroup O3a1c-002611. Int J Syst Evol 2013, 51:280-286.
• [78]Mirabal S, Herrera KJ, Gayden T, Regueiro M, Underhill PA, Garcia-Bertrand RL, Herrera RJ: Increased Y-chromosome resolution of haplogroup O suggests genetic ties between the Ami aborigines of Taiwan and the Polynesian Islands of Samoa and Tonga. Gene 2012, 492:339-348.
• [79]Pierson MJ, Martinez-Arias R, Holland BR, Gemmell NJ, Hurles ME, Penny D: Deciphering past human population movements in Oceania: provably optimal trees of 127 mtDNA genomes. Mol Biol Evol 2006, 23:1966-1975.
• [80]Mona S, Grunz KE, Brauer S, Pakendorf B, Castri L, Sudoyo H, Marzuki S, Barnes RH, Schmidtke J, Stoneking M, Kayser M: Genetic admixture history of Eastern Indonesia as revealed by Y-chromosome and mitochondrial DNA analysis. Mol Biol Evol 2009, 26:1865-1877.
• [81]Delfin F, Myles S, Choi Y, Hughes D, Illek R, van Oven M, Pakendorf B, Kayser M, Stoneking M: Bridging near and remote Oceania: mtDNA and NRY variation in the Solomon Islands. Mol Biol Evol 2012, 29:545-564.
• [82]Solheim WG: Archaeology and Culture in Southeast Asia: Unraveling the Nusantao. Diliman, Quezon City: University of the Philippines Press; 2006:316. ISBN 971-542-508-9
• [83]Tsang CH: The prehistory of Taiwan: a brief introduction. In Seventeenth Congress of the Indo-Pacific Prehistory Association; Sep 9–15. Taipei (Taiwan): Academia Sinica; 2002:47-52.
• [84]Zhong H, Shi H, Qi XB, Duan ZY, Tan PP, Jin L, Su B, Ma RZ: Extended Y chromosome investigation suggests postglacial migrations of modern humans into East Asia via the northern route. Mol Biol Evol 2011, 28:717-727.
• [85]Sharma S, Rai E, Bhat AK, Bhanwer AS, Bamezai RN: A novel subgroup Q5 of human Y-chromosomal haplogroup Q in India. BMC Evol Biol 2007, 7:232.
• [86]Razafindrazaka H, Ricaut F, Cox M, Mormina M, Dugoujon J, Randriamarolaza L, Guitard E, Tonasso L, Ludes B, Crubezy E: Complete mitochondrial DNA sequences provide new insights into the Polynesian motif and the peopling of Madagascar. Eur J Hum Genet 2010, 18:575-581.
• [87]Abdulla MA, Ahmed I, Assawamakin A, Bhak J, Brahmachari SK, Calacal GC, Chaurasia A, Chen CH, Chen J, Chen YT, Chu J, la Paz EM C-d, De Ungria MC, Delfin FC, Edo J, Fuchareon S, Ghang H, Gojobori T, Han J, Ho SF, Hoh BP, Huang W, Inoko H, Jha P, Jinam TA, Jin L, Jung J, Kangwanpong D, Kampuansai J, Kennedy GC: Mapping human genetic diversity in Asia. Science 2009, 326:1541-1545.