Native American Mitochondrial DNA Analysis Indicates That the Amerind and the Nadene Populations Were Founded by Two Independent Migrations (original) (raw)

Abstract

Mitochondrial DNAs (mtDNAs) from 167 American Indians including 87 Amerind-speakers (Amerinds) and 80 Nadene-speakers (Nadene) were surveyed for sequence variation by detailed restriction analysis. All Native American mtDNAs clustered into one of four distinct lineages, defined by the restriction site variants: HincII site loss at np 13,259, AluI site loss at np 5,176, 9-base pair (9-bp) COII-tRNA(Lys) intergenic deletion and HaeIII site gain at np 663. The HincII np 13,259 and AluI np 5,176 lineages were observed exclusively in Amerinds and were shared by all such tribal groups analyzed, thus demonstrating that North, Central and South American Amerinds originated from a common ancestral genetic stock. The 9-bp deletion and HaeIII np 663 lineages were found in both the Amerinds and Nadene but the Nadene HaeIII np 663 lineage had a unique sublineage defined by an RsaI site loss at np 16,329. The amount of sequence variation accumulated in the Amerind HincII np 13,259 and AluI np 5,176 lineages and that in the Amerind portion of the HaeIII np 663 lineage all gave divergence times in the order of 20,000 years before present. The divergence time for the Nadene portion of the HaeIII np 663 lineage was about 6,000-10,000 years. Hence, the ancestral Nadene migrated from Asia independently and considerably more recently than the progenitors of the Amerinds. The divergence times of both the Amerind and Nadene branches of the COII-tRNA(Lys) deletion lineage were intermediate between the Amerind and Nadene specific lineages, raising the possibility of a third source of mtDNA in American Indians.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  2. Ballinger S. W., Schurr T. G., Torroni A., Gan Y. Y., Hodge J. A., Hassan K., Chen K. H., Wallace D. C. Southeast Asian mitochondrial DNA analysis reveals genetic continuity of ancient mongoloid migrations. Genetics. 1992 Jan;130(1):139–152. doi: 10.1093/genetics/130.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blanc H., Chen K. H., D'Amore M. A., Wallace D. C. Amino acid change associated with the major polymorphic Hinc II site of Oriental and Caucasian mitochondrial DNAs. Am J Hum Genet. 1983 Mar;35(2):167–176. [PMC free article] [PubMed] [Google Scholar]
  4. Brown M. D., Voljavec A. S., Lott M. T., Torroni A., Yang C. C., Wallace D. C. Mitochondrial DNA complex I and III mutations associated with Leber's hereditary optic neuropathy. Genetics. 1992 Jan;130(1):163–173. doi: 10.1093/genetics/130.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brown W. M. Polymorphism in mitochondrial DNA of humans as revealed by restriction endonuclease analysis. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3605–3609. doi: 10.1073/pnas.77.6.3605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cann R. L., Wilson A. C. Length mutations in human mitochondrial DNA. Genetics. 1983 Aug;104(4):699–711. doi: 10.1093/genetics/104.4.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Giles R. E., Blanc H., Cann H. M., Wallace D. C. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6715–6719. doi: 10.1073/pnas.77.11.6715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Greenberg B. D., Newbold J. E., Sugino A. Intraspecific nucleotide sequence variability surrounding the origin of replication in human mitochondrial DNA. Gene. 1983 Jan-Feb;21(1-2):33–49. doi: 10.1016/0378-1119(83)90145-2. [DOI] [PubMed] [Google Scholar]
  10. Harihara S., Hirai M., Omoto K. Mitochondrial DNA polymorphism in Japanese living in Hokkaido. Jinrui Idengaku Zasshi. 1986 Jun;31(2):73–83. doi: 10.1007/BF01871401. [DOI] [PubMed] [Google Scholar]
  11. Harihara S., Saitou N., Hirai M., Gojobori T., Park K. S., Misawa S., Ellepola S. B., Ishida T., Omoto K. Mitochondrial DNA polymorphism among five Asian populations. Am J Hum Genet. 1988 Aug;43(2):134–143. [PMC free article] [PubMed] [Google Scholar]
  12. Hertzberg M., Mickleson K. N., Serjeantson S. W., Prior J. F., Trent R. J. An Asian-specific 9-bp deletion of mitochondrial DNA is frequently found in Polynesians. Am J Hum Genet. 1989 Apr;44(4):504–510. [PMC free article] [PubMed] [Google Scholar]
  13. Horai S., Gojobori T., Matsunaga E. Mitochondrial DNA polymorphism in Japanese. I. Analysis with restriction enzymes of six base pair recognition. Hum Genet. 1984;68(4):324–332. doi: 10.1007/BF00292594. [DOI] [PubMed] [Google Scholar]
  14. Horai S., Matsunaga E. Mitochondrial DNA polymorphism in Japanese. II. Analysis with restriction enzymes of four or five base pair recognition. Hum Genet. 1986 Feb;72(2):105–117. doi: 10.1007/BF00283927. [DOI] [PubMed] [Google Scholar]
  15. Johnson M. J., Wallace D. C., Ferris S. D., Rattazzi M. C., Cavalli-Sforza L. L. Radiation of human mitochondria DNA types analyzed by restriction endonuclease cleavage patterns. J Mol Evol. 1983;19(3-4):255–271. doi: 10.1007/BF02099973. [DOI] [PubMed] [Google Scholar]
  16. Knowler W. C., Bennett P. H., Hamman R. F., Miller M. Diabetes incidence and prevalence in Pima Indians: a 19-fold greater incidence than in Rochester, Minnesota. Am J Epidemiol. 1978 Dec;108(6):497–505. doi: 10.1093/oxfordjournals.aje.a112648. [DOI] [PubMed] [Google Scholar]
  17. Marshall E. Clovis Counterrevolution: The debate on who came first to the Americas, and where they lived, seems headed for a new round as the skeptics strike at "pre-Clovis" discoveries. Science. 1990 Aug 17;249(4970):738–741. doi: 10.1126/science.249.4970.738. [DOI] [PubMed] [Google Scholar]
  18. Matson G. A., Burch T. A., Polesky H. F., Swanson J., Sutton H. E., Robinson A. Distribution of hereditary factors in the blood of Indians of the Gila River, Arizona. Am J Phys Anthropol. 1968 Nov;29(3):311–337. doi: 10.1002/ajpa.1330290308. [DOI] [PubMed] [Google Scholar]
  19. Miyata T., Hayashida H., Kikuno R., Hasegawa M., Kobayashi M., Koike K. Molecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol. 1982;19(1):28–35. doi: 10.1007/BF02100221. [DOI] [PubMed] [Google Scholar]
  20. Neel J. V., Gershowitz H., Mohrenweiser H. W., Amos B., Kostyu D. D., Salzano F. M., Mestriner M. A., Lawrence D., Simões A. L., Smouse P. E. Genetic studies on the Ticuna, an enigmatic tribe of Central Amazonas. Ann Hum Genet. 1980 Jul;44(Pt 1):37–54. doi: 10.1111/j.1469-1809.1980.tb00944.x. [DOI] [PubMed] [Google Scholar]
  21. Neel J. V. Rare variants, private polymorphisms, and locus heterozygosity in Amerindian populations. Am J Hum Genet. 1978 Sep;30(5):465–490. [PMC free article] [PubMed] [Google Scholar]
  22. Neel J. V., Thompson E. A. Founder effect and number of private polymorphisms observed in Amerindian tribes. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1904–1908. doi: 10.1073/pnas.75.4.1904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nei M., Tajima F. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics. 1983 Sep;105(1):207–217. doi: 10.1093/genetics/105.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nelson D. E., Morlan R. E., Vogel J. S., Southon J. R., Harington C. R. New dates on northern yukon artifacts: holocene not upper pleistocene. Science. 1986 May 9;232(4751):749–751. doi: 10.1126/science.232.4751.749. [DOI] [PubMed] [Google Scholar]
  25. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  26. Schurr T. G., Ballinger S. W., Gan Y. Y., Hodge J. A., Merriwether D. A., Lawrence D. N., Knowler W. C., Weiss K. M., Wallace D. C. Amerindian mitochondrial DNAs have rare Asian mutations at high frequencies, suggesting they derived from four primary maternal lineages. Am J Hum Genet. 1990 Mar;46(3):613–623. [PMC free article] [PubMed] [Google Scholar]
  27. Stoneking M., Bhatia K., Wilson A. C. Rate of sequence divergence estimated from restriction maps of mitochondrial DNAs from Papua New Guinea. Cold Spring Harb Symp Quant Biol. 1986;51(Pt 1):433–439. doi: 10.1101/sqb.1986.051.01.052. [DOI] [PubMed] [Google Scholar]
  28. Stoneking M., Jorde L. B., Bhatia K., Wilson A. C. Geographic variation in human mitochondrial DNA from Papua New Guinea. Genetics. 1990 Mar;124(3):717–733. doi: 10.1093/genetics/124.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Szathmary E. J. Dogrib Indians of the Northwest Territories, Canada: genetic diversity and genetic relationship among subarctic Indians. Ann Hum Biol. 1983 Mar-Apr;10(2):147–162. doi: 10.1080/03014468300006291. [DOI] [PubMed] [Google Scholar]
  30. Szathmary E. J., Ferrell R. E., Gershowitz H. Genetic differentiation in Dogrib Indians: serum protein and erythrocyte enzyme variation. Am J Phys Anthropol. 1983 Nov;62(3):249–254. doi: 10.1002/ajpa.1330620304. [DOI] [PubMed] [Google Scholar]
  31. Szathmary E. J. Peopling of northern North America: clues from genetic studies. Acta Anthropogenet. 1984;8(1-2):79–109. [PubMed] [Google Scholar]
  32. Szathmary E. J., Ritenbaugh C., Goodby C. S. Dietary change and plasma glucose levels in an Amerindian population undergoing cultural transition. Soc Sci Med. 1987;24(10):791–804. doi: 10.1016/0277-9536(87)90181-x. [DOI] [PubMed] [Google Scholar]
  33. Troup G. M., Schanfield M. S., Singaraju C. H., Harvey R. L., Jameson J., Capper J., Baker B. Study of HLA alloantigens of the Navajo Indians of North America. II. HLA-A, B, C, DR and other genetic markers. Tissue Antigens. 1982 Nov;20(5):339–351. doi: 10.1111/j.1399-0039.1982.tb02250.x. [DOI] [PubMed] [Google Scholar]
  34. Vigilant L., Pennington R., Harpending H., Kocher T. D., Wilson A. C. Mitochondrial DNA sequences in single hairs from a southern African population. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9350–9354. doi: 10.1073/pnas.86.23.9350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wallace D. C., Garrison K., Knowler W. C. Dramatic founder effects in Amerindian mitochondrial DNAs. Am J Phys Anthropol. 1985 Oct;68(2):149–155. doi: 10.1002/ajpa.1330680202. [DOI] [PubMed] [Google Scholar]
  36. Wallace D. C., Singh G., Lott M. T., Hodge J. A., Schurr T. G., Lezza A. M., Elsas L. J., 2nd, Nikoskelainen E. K. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science. 1988 Dec 9;242(4884):1427–1430. doi: 10.1126/science.3201231. [DOI] [PubMed] [Google Scholar]
  37. Wallace D. C., Ye J. H., Neckelmann S. N., Singh G., Webster K. A., Greenberg B. D. Sequence analysis of cDNAs for the human and bovine ATP synthase beta subunit: mitochondrial DNA genes sustain seventeen times more mutations. Curr Genet. 1987;12(2):81–90. doi: 10.1007/BF00434661. [DOI] [PubMed] [Google Scholar]
  38. Williams R. C., Morse H. G., Bonnell M. D., Rate R. G., Kuberski T. T. The HLA loci of th Hopi and Navajo. Am J Phys Anthropol. 1981 Nov;56(3):291–296. doi: 10.1002/ajpa.1330560309. [DOI] [PubMed] [Google Scholar]
  39. Williams R. C., Steinberg A. G., Gershowitz H., Bennett P. H., Knowler W. C., Pettitt D. J., Butler W., Baird R., Dowda-Rea L., Burch T. A. GM allotypes in Native Americans: evidence for three distinct migrations across the Bering land bridge. Am J Phys Anthropol. 1985 Jan;66(1):1–19. doi: 10.1002/ajpa.1330660102. [DOI] [PubMed] [Google Scholar]
  40. Williams R. C., Steinberg A. G., Knowler W. C., Pettitt D. J. Gm 3;5,13,14 and stated-admixture: independent estimates of admixture in American Indians. Am J Hum Genet. 1986 Sep;39(3):409–413. [PMC free article] [PubMed] [Google Scholar]
  41. Wrischnik L. A., Higuchi R. G., Stoneking M., Erlich H. A., Arnheim N., Wilson A. C. Length mutations in human mitochondrial DNA: direct sequencing of enzymatically amplified DNA. Nucleic Acids Res. 1987 Jan 26;15(2):529–542. doi: 10.1093/nar/15.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]