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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Apr 30;93(9):4360–4364. doi: 10.1073/pnas.93.9.4360

DNA sequences of Alu elements indicate a recent replacement of the human autosomal genetic complement.

A Knight 1, M A Batzer 1, M Stoneking 1, H K Tiwari 1, W D Scheer 1, R J Herrera 1, P L Deininger 1
PMCID: PMC39542  PMID: 8633071

Abstract

DNA sequences of neutral nuclear autosomal loci, compared across diverse human populations, provide a previously untapped perspective into the mode and tempo of the emergence of modern humans and a critical comparison with published clonally inherited mitochondrial DNA and Y chromosome measurements of human diversity. We obtained over 55 kilobases of sequence from three autosomal loci encompassing Alu repeats for representatives of diverse human populations as well as orthologous sequences for other hominoid species at one of these loci. Nucleotide diversity was exceedingly low. Most individuals and populations were identical. Only a single nucleotide difference distinguished presumed ancestral alleles from descendants. These results differ from those expected if alleles from divergent archaic populations were maintained through multiregional continuity. The observed virtual lack of sequence polymorphism is the signature of a recent single origin for modern humans, with general replacement of archaic populations.

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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. Antonarakis S. E., Oettgen P., Chakravarti A., Halloran S. L., Hudson R. R., Feisee L., Karathanasis S. K. DNA polymorphism haplotypes of the human apolipoprotein APOA1-APOC3-APOA4 gene cluster. Hum Genet. 1988 Nov;80(3):265–273. doi: 10.1007/BF01790095. [DOI] [PubMed] [Google Scholar]
  3. Bailey W. J., Hayasaka K., Skinner C. G., Kehoe S., Sieu L. C., Slightom J. L., Goodman M. Reexamination of the African hominoid trichotomy with additional sequences from the primate beta-globin gene cluster. Mol Phylogenet Evol. 1992 Jun;1(2):97–135. doi: 10.1016/1055-7903(92)90024-b. [DOI] [PubMed] [Google Scholar]
  4. Batzer M. A., Stoneking M., Alegria-Hartman M., Bazan H., Kass D. H., Shaikh T. H., Novick G. E., Ioannou P. A., Scheer W. D., Herrera R. J. African origin of human-specific polymorphic Alu insertions. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12288–12292. doi: 10.1073/pnas.91.25.12288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowcock A. M., Kidd J. R., Mountain J. L., Hebert J. M., Carotenuto L., Kidd K. K., Cavalli-Sforza L. L. Drift, admixture, and selection in human evolution: a study with DNA polymorphisms. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):839–843. doi: 10.1073/pnas.88.3.839. [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., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
  8. Carothers A. M., Urlaub G., Mucha J., Grunberger D., Chasin L. A. Point mutation analysis in a mammalian gene: rapid preparation of total RNA, PCR amplification of cDNA, and Taq sequencing by a novel method. Biotechniques. 1989 May;7(5):494-6, 498-9. [PubMed] [Google Scholar]
  9. Carr S. M., Ballinger S. W., Derr J. N., Blankenship L. H., Bickham J. W. Mitochondrial DNA analysis of hybridization between sympatric white-tailed deer and mule deer in west Texas. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9576–9580. doi: 10.1073/pnas.83.24.9576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dorit R. L., Akashi H., Gilbert W. Absence of polymorphism at the ZFY locus on the human Y chromosome. Science. 1995 May 26;268(5214):1183–1185. doi: 10.1126/science.7761836. [DOI] [PubMed] [Google Scholar]
  11. Ferris S. D., Sage R. D., Huang C. M., Nielsen J. T., Ritte U., Wilson A. C. Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2290–2294. doi: 10.1073/pnas.80.8.2290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fullerton S. M., Harding R. M., Boyce A. J., Clegg J. B. Molecular and population genetic analysis of allelic sequence diversity at the human beta-globin locus. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1805–1809. doi: 10.1073/pnas.91.5.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gabunia L., Vekua A. A Plio-Pleistocene hominid from Dmanisi, East Georgia, Caucasus. Nature. 1995 Feb 9;373(6514):509–512. doi: 10.1038/373509a0. [DOI] [PubMed] [Google Scholar]
  14. Gonzalez I. L., Petersen R., Sylvester J. E. Independent insertion of Alu elements in the human ribosomal spacer and their concerted evolution. Mol Biol Evol. 1989 Jul;6(4):413–423. doi: 10.1093/oxfordjournals.molbev.a040554. [DOI] [PubMed] [Google Scholar]
  15. Gyllensten U., Wilson A. C. Interspecific mitochondrial DNA transfer and the colonization of Scandinavia by mice. Genet Res. 1987 Feb;49(1):25–29. doi: 10.1017/s0016672300026690. [DOI] [PubMed] [Google Scholar]
  16. Horai S., Satta Y., Hayasaka K., Kondo R., Inoue T., Ishida T., Hayashi S., Takahata N. Man's place in Hominoidea revealed by mitochondrial DNA genealogy. J Mol Evol. 1992 Jul;35(1):32–43. doi: 10.1007/BF00160258. [DOI] [PubMed] [Google Scholar]
  17. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  18. Kraus F., Miyamoto M. M. Mitochondrial genotype of a unisexual salamander of hybrid origin is unrelated to either of its nuclear haplotypes. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2235–2238. doi: 10.1073/pnas.87.6.2235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kurth J. H., Cavalli-Sforza L. L. Notes on individual sequence variation in humans: immunoglobulin kappa light chain. Am J Hum Genet. 1994 Jun;54(6):1037–1041. [PMC free article] [PubMed] [Google Scholar]
  20. Kurth J. H., Mountain J. L., Cavalli-Sforza L. L. Subclustering of human immunoglobulin kappa light chain variable region genes. Genomics. 1993 Apr;16(1):69–77. doi: 10.1006/geno.1993.1142. [DOI] [PubMed] [Google Scholar]
  21. Li W. H., Sadler L. A. Low nucleotide diversity in man. Genetics. 1991 Oct;129(2):513–523. doi: 10.1093/genetics/129.2.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Livshits G., Nei M. Relationships between intrapopulational and interpopulational genetic diversity in man. Ann Hum Biol. 1990 Nov-Dec;17(6):501–513. doi: 10.1080/03014469000001272. [DOI] [PubMed] [Google Scholar]
  23. Nei M., Li W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5269–5273. doi: 10.1073/pnas.76.10.5269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nei M., Livshits G. Genetic relationships of Europeans, Asians and Africans and the origin of modern Homo sapiens. Hum Hered. 1989;39(5):276–281. doi: 10.1159/000153872. [DOI] [PubMed] [Google Scholar]
  25. Powell J. R. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci U S A. 1983 Jan;80(2):492–495. doi: 10.1073/pnas.80.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Saluz H., Jost J. P. A simple high-resolution procedure to study DNA methylation and in vivo DNA-protein interactions on a single-copy gene level in higher eukaryotes. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2602–2606. doi: 10.1073/pnas.86.8.2602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sawada I., Willard C., Shen C. K., Chapman B., Wilson A. C., Schmid C. W. Evolution of Alu family repeats since the divergence of human and chimpanzee. J Mol Evol. 1985;22(4):316–322. doi: 10.1007/BF02115687. [DOI] [PubMed] [Google Scholar]
  28. Spolsky C., Uzzell T. Natural interspecies transfer of mitochondrial DNA in amphibians. Proc Natl Acad Sci U S A. 1984 Sep;81(18):5802–5805. doi: 10.1073/pnas.81.18.5802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Swisher C. C., 3rd, Curtis G. H., Jacob T., Getty A. G., Suprijo A., Widiasmoro Age of the earliest known hominids in Java, Indonesia. Science. 1994 Feb 25;263(5150):1118–1121. doi: 10.1126/science.8108729. [DOI] [PubMed] [Google Scholar]
  30. Takahata N. Allelic genealogy and human evolution. Mol Biol Evol. 1993 Jan;10(1):2–22. doi: 10.1093/oxfordjournals.molbev.a039995. [DOI] [PubMed] [Google Scholar]
  31. Tegelström H. Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus). J Mol Evol. 1987;24(3):218–227. doi: 10.1007/BF02111235. [DOI] [PubMed] [Google Scholar]
  32. Tiret L., Rigat B., Visvikis S., Breda C., Corvol P., Cambien F., Soubrier F. Evidence, from combined segregation and linkage analysis, that a variant of the angiotensin I-converting enzyme (ACE) gene controls plasma ACE levels. Am J Hum Genet. 1992 Jul;51(1):197–205. [PMC free article] [PubMed] [Google Scholar]
  33. Vigilant L., Stoneking M., Harpending H., Hawkes K., Wilson A. C. African populations and the evolution of human mitochondrial DNA. Science. 1991 Sep 27;253(5027):1503–1507. doi: 10.1126/science.1840702. [DOI] [PubMed] [Google Scholar]

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