Journal of Human Genetics

, Volume 50, Issue 10, pp 497–506 | Cite as

Human mtDNA hypervariable regions, HVR I and II, hint at deep common maternal founder and subsequent maternal gene flow in Indian population groups

  • Swarkar Sharma
  • Anjana Saha
  • Ekta Rai
  • Audesh Bhat
  • Ramesh Bamezai
Original Article

Abstract

We have analysed the hypervariable regions (HVR I and II) of human mitochondrial DNA (mtDNA) in individuals from Uttar Pradesh (UP), Bihar (BI) and Punjab (PUNJ), belonging to the Indo-European linguistic group, and from South India (SI), that have their linguistic roots in Dravidian language. Our analysis revealed the presence of known and novel mutations in both hypervariable regions in the studied population groups. Median joining network analyses based on mtDNA showed extensive overlap in mtDNA lineages despite the extensive cultural and linguistic diversity. MDS plot analysis based on Fst distances suggested increased maternal genetic proximity for the studied population groups compared with other world populations. Mismatch distribution curves, respective neighbour joining trees and other statistical analyses showed that there were significant expansions. The study revealed an ancient common ancestry for the studied population groups, most probably through common founder female lineage(s), and also indicated that human migrations occurred (maybe across and within the Indian subcontinent) even after the initial phase of female migration to India.

Keywords

Indian populations Mitochondrial DNA Matrilineal HVR I and II 

References

  1. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465CrossRefPubMedGoogle Scholar
  2. Bamshad M, Kivisild T, Watkins WS, Dixon ME, Ricker CE, Rao BB, Naidu JM, Prasad BV, Reddy PG, Rasanayagam A, Papiha SS, Villems R, Redd AJ, Hammer MF, Nguyen SV, Carroll ML, Batzer MA, Jorde LB (2001) Genetic evidence on the origins of Indian caste populations. Genome Res 11:994–1004CrossRefPubMedGoogle Scholar
  3. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  4. Basu A, Mukherjee N, Roy S, Sengupta S, Banerjee S, Chakraborty M, Dey B, Roy M, Roy B, Bhattacharyya NP, Roychoudhury S, Majumder PP (2003) Ethnic India: a genomic view, with special reference to peopling and structure. Genome Res 13:2277–2290CrossRefPubMedGoogle Scholar
  5. Brandon MC, Lott MT, Nguyen KC, Spolim S, Navathe SB, Baldi P, Wallace DC (2005) MITOMAP: a human mitochondrial genome database: 2004 update. Nucleic Acids Res 33:D611–D613 (see also http://www.mitomap.org)CrossRefPubMedGoogle Scholar
  6. Budowle B, Allard MW, Wilson MR (2002) Critique of interpretation of high levels of heteroplasmy in the human mitochondrial DNA hypervariable region I from hair. Forensic Sci Int 126:30–33CrossRefPubMedGoogle Scholar
  7. Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325:31–36CrossRefPubMedGoogle Scholar
  8. Crouau-Roy B, Service S, Slatkin M, Freimer N (1996) A fine-scale comparison of the human and chimpanzee genomes: linkage, linkage disequilibrium and sequence analysis. Hum Mol Genet 5:1131–1137CrossRefPubMedGoogle Scholar
  9. Derbeneva OA, Sukernik RI, Volodko NV, Hosseini SH, Lott MT, Wallace DC (2002) Analysis of mitochondrial DNA diversity in the aleuts of the Commander Islands and its implications for the genetic history of Beringia. Am J Hum Genet 71:415–421CrossRefPubMedGoogle Scholar
  10. Felsenstein J (1989) PHYLIP—Phylogeny Inference Package (version 3.2). Cladistics 5:164–166Google Scholar
  11. Forster P, Harding R, Torroni A, Bandelt HJ (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet 59:935–945PubMedGoogle Scholar
  12. Forster P, Matsumura S (2005) Evolution: Did early humans go north or south? Science 308:965–966CrossRefPubMedGoogle Scholar
  13. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  14. Greenberg BD, Newbold JE, Sugino A (1983) Intraspecific nucleotide sequence variability surrounding the origin of replication in human mitochondrial DNA. Gene 21:33–49CrossRefPubMedGoogle Scholar
  15. Gresham D, Morar B, Underhill PA, Passarino G, Lin AA, Wise C, Angelicheva D, Calafell F, Oefner PJ, Shen P, Tournev I, de Pablo R, Kucinskas V, Perez-Lezaun A, Marushiakova E, Popov V, Kalaydjieva L (2001) Origins and divergence of the Roma (gypsies). Am J Hum Genet 69:1314–1331CrossRefPubMedGoogle Scholar
  16. Houck MM, Budowle B (2002) Correlation of microscopic and mitochondrial DNA hair comparisons. J Forensic Sci 47:964–967PubMedGoogle Scholar
  17. Ingman M, Gyllensten U (2001) Analysis of the complete human mtDNA genome: methodology and inferences for human evolution. J Hered 92:454–461CrossRefPubMedGoogle Scholar
  18. Kaessmann H, Wiebe V, Paabo S (1999) Extensive nuclear DNA sequence diversity among chimpanzees. Science 286:1159–1162CrossRefPubMedGoogle Scholar
  19. Kaur I, Roy S, Chakrabarti S, Sarhadi VK, Majumder PP, Bhanwer AJ, Singh JR (2002) Genomic diversities and affinities among four endogamous groups of Punjab (India) based on autosomal and mitochondrial DNA polymorphisms. Hum Biol 74:819–836PubMedGoogle Scholar
  20. Kivisild T, Bamshad MJ, Kaldma K, Metspalu M, Metspalu E, Reidla M, Laos S, Parik J, Watkins WS, Dixon ME, Papiha SS, Mastana SS, Mir MR, Ferak V, Villems R (1999) Deep common ancestry of Indian and western-Eurasian mitochondrial DNA lineages. Curr Biol 9:1331–1334CrossRefPubMedGoogle Scholar
  21. Kivisild T, Rootsi S, Metspalu M, Mastana S, Kaldma K, Parik J, Metspalu E, Adojaan M, Tolk HV, Stepanov V, Golge M, Usanga E, Papiha SS, Cinnioglu C, King R, Cavalli-Sforza L, Underhill PA, Villems R (2003) The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations. Am J Hum Genet 72:313–332CrossRefPubMedGoogle Scholar
  22. Koyama H, Iwasa M, Ohtani S, Ohira H, Tsuchimochi T, Maeno Y, Isobe I, Matsumoto T, Yamada Y, Nagao M (2002) Personal identification from human remains by mitochondrial DNA sequencing. Am J Forensic Med Pathol 23:272–276CrossRefPubMedGoogle Scholar
  23. Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Arizona State University, Tempe, AZGoogle Scholar
  24. Kunkel LM, Smith KD, Boyer SH, Bargaonkar DS (1977) Analysis of human Y chromosome specific reiterated DNA in chromosome variants. P Natl Acad Sci USA 74:1245–1249Google Scholar
  25. Li WH, Sadler LA (1991) Low nucleotide diversity in man. Genetics 129:513–523PubMedGoogle Scholar
  26. Macaulay V, Hill C, Achilli A, Rengo C, Clarke D, Meehan W, Blackburn J, Semino O, Scozzari R, Cruciani F, Taha A, Shaari NK, Raja JM, Ismail P, Zainuddin Z, Goodwin W, Bulbeck D, Bandelt HJ, Oppenheimer S, Torroni A, Richards M (2005) Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308:1034–1036CrossRefPubMedGoogle Scholar
  27. Melton T, Wilson M, Batzer M, Stoneking M (1997) Extent of heterogeneity in mitochondrial DNA of European populations. J Forensic Sci 42:437–446PubMedGoogle Scholar
  28. Metspalu M, Kivisild T, Metspalu E, Parik J, Hudjashov G, Kaldma K, Serk P, Karmin M, Behar DM, Gilbert MT, Endicott P, Mastana S, Papiha SS, Skorecki K, Torroni A, Villems R (2004) Most of the extant mtDNA boundaries in south and southwest Asia were likely shaped during the initial settlement of Eurasia by anatomically modern humans. BMC Genet 5:26CrossRefPubMedGoogle Scholar
  29. Palanichamy MG, Sun C, Agrawal S, Bandelt HJ, Kong QP, Khan F, Wang CY, Chaudhuri TK, Palla V, Zhang YP (2004) Phylogeny of mitochondrial DNA macrohaplogroup N in India, based on complete sequencing: implications for the peopling of South Asia. Am J Hum Genet 75:966–978CrossRefPubMedGoogle Scholar
  30. Passarino G, Semino O, Bernini LF, Santachiara-Benerecetti AS (1996) Pre-caucasoid and caucasoid genetic features of the Indian population, revealed by mtDNA polymorphisms. Am J Hum Genet 59: 927-34PubMedGoogle Scholar
  31. Quintana-Murci L, Semino O, Bandelt HJ, Passarino G, McElreavey K, Santachiara-Benerecetti AS (1999) Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nat Genet 23:437–441CrossRefPubMedGoogle Scholar
  32. Quintana-Murci L, Krausz C, Zerjal T, Sayar SH, Hammer MF, Mehdi SQ, Ayub Q, Qamar R, Mohyuddin A, Radhakrishna U, Jobling MA, Tyler-Smith C, McElreavey K (2001) Y-chromosome lineages trace diffusion of people and languages in southwestern Asia. Am J Hum Genet 68:537–542CrossRefPubMedGoogle Scholar
  33. Rajkumar R, Kashyap VK (2003) Haplotype diversity in mitochondrial DNA hypervariable regions I and II in three communities of Southern India. Forensic Sci Int 136:79–82CrossRefPubMedGoogle Scholar
  34. Rajkumar R, Banerjee J, Gunturi HB, Trivedi R, Kashyap VK (2005) Phylogeny and antiquity of M macrohaplogroup inferred from complete mtDNA sequence of Indian specific lineages. BMC Evol Biol 5:26CrossRefPubMedGoogle Scholar
  35. Richards M, Rengo C, Cruciani F, Gratrix F, Wilson JF, Scozzari R, Macaulay V, Torroni A (2003) Extensive female-mediated gene flow from sub-Saharan Africa into near eastern Arab populations. Am J Hum Genet 72:1058–1064CrossRefPubMedGoogle Scholar
  36. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  37. Roychoudhury S, Roy S, Dey B, Chakraborty M, Roy M, Roy B, Ramesh A, Prabhakaran N, Rani MVU, Vishwanathan HMM (2000) Fundamental genomic unity of ethnic India is revealed by analysis of mitochondrial DNA. Curr Sci 79:1182–1192Google Scholar
  38. Roychoudhury S, Roy S, Basu A, Banerjee R, Vishwanathan H, Usha Rani MV, Sil SK, Mitra M, Majumder PP (2001) Genomic structures and population histories of linguistically distinct tribal groups of India. Hum Genet 109:339–350CrossRefPubMedGoogle Scholar
  39. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175CrossRefPubMedGoogle Scholar
  40. Saha A, Sharma S, Bhat A, Pandit A, Bamezai R (2005) Genetic affinity among five different population groups in India reflecting a Y-chromosome gene flow. J Hum Genet 50:49–51CrossRefPubMedGoogle Scholar
  41. Schneider S, Roessli D, Excoffier L (2000) Arlequin version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  42. Seo Y, Uchiyama T, Matsuda H, Shimizu K, Takami Y, Nakayama T, Takahama K (2002) Mitochondrial DNA and STR typing of matter adhering to an earphone. J Forensic Sci 47:605–608PubMedGoogle Scholar
  43. Sherry ST, Rogers AR, Harpending H, Soodyall H, Jenkins T, Stoneking M (1994) Mismatch distributions of mtDNA reveal recent human population expansions. Hum Biol 66:761–775PubMedGoogle Scholar
  44. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  45. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  46. Thangaraj K, Chaubey G, Kivisild T, Reddy AG, Singh VK, Rasalkar AA, Singh L (2005) Reconstructing the origin of Andaman Islanders. Science 308:996CrossRefPubMedGoogle Scholar
  47. Yao YG, Nie L, Harpending H, Fu YX, Yuan ZG, Zhang YP (2002) Genetic relationship of Chinese ethnic populations revealed by mtDNA sequence diversity. Am J Phys Anthropol 118:63–76CrossRefPubMedGoogle Scholar
  48. Yao YG, Zhang YP (2002) Phylogeographic analysis of mtDNA variation in four ethnic populations from Yunnan Province: new data and a reappraisal. J Hum Genet 47:311–318CrossRefPubMedGoogle Scholar

Copyright information

© The Japan Society of Human Genetics and Springer-Verlag 2005

Authors and Affiliations

  • Swarkar Sharma
    • 1
  • Anjana Saha
    • 1
  • Ekta Rai
    • 1
  • Audesh Bhat
    • 1
  • Ramesh Bamezai
    • 1
  1. 1.National Centre of Applied Human Genetics, School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia

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