Journal of Molecular Evolution

, Volume 42, Issue 1, pp 22–29

Genetic variation of recent Alu insertions in human populations

  • Mark A. Batzer
  • Santosh S. Arcot
  • Joshua W. Phinney
  • Michelle Alegria-Hartman
  • David H. Kass
  • Stephen M. Milligan
  • Colin Kimpton
  • Peter Gill
  • Manfred Hochmeister
  • Panayiotis A. Ioannou
  • Rene J. Herrera
  • Donald A. Boudreau
  • W. Douglas Scheer
  • Bronya J. B. Keats
  • Prescott L. Deininger
  • Mark Stoneking
Articles

Abstract

The Alu family of intersperesed repeats is comprised of ovr 500,000 members which may be divided into discrete subfamilies based upon mutations held in common between members. Distinct subfamilies of Alu sequences have amplified within the human genome in recent evolutionary history. Several individual Alu family members have amplified so recently in human evolution that they are variable as to presence and absence at specific loci within different human populations. Here, we report on the distribution of six polymorphic Alu insetions in a survey of 563 individuals from 14 human population groups across several continents. Our results indicate that these polymorphic Alu insertions probably have an African origin and that there is a much smaller amount of genetic variation between European populations than that found between other populations groups.

Key words

Human evolution African origin Identical by descent Polymorphism 

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References

  1. Ausabel FM, Brent R, Kingston RE, More DD, Seidman JG, Smith JA, Struhl K (eds) (1987) Current protocols in Molecular Biology. John Wiley and Sons, New YorkGoogle Scholar
  2. Bailey AD, Shen C-KJ (1993) Sequential insertion of Alu family repeats into specific genomic sites of higher primates. Proc Nail Acad Sci USA 90:7205–7209Google Scholar
  3. Batzer MA, Deininger PL (1991) A human-specific subfamily of Alu sequences. Genomics 9:481–487Google Scholar
  4. Batzer MA, Kilroy GE, Richard PE, Shaikh TH, Desselle TD, Hoppens CL, Deininger PL (1990) Structure and variability of recently inserted Alu family members. Nucleic Acids Res 18:6793–6798Google Scholar
  5. Batzer MA, Gudi VA, Mena JC, Foltz DW, Herrera RJ, Deininger PL (1991) Amplification dynamics of Human-Specific (HS) Alu family members. Nucleic Acids Res 19:3619–3623Google Scholar
  6. Batzer MA, Stoneking M, Alegria-Hartman M, Bazan H, Kass DH, Shaikh TH, Novick GE, Ioannou PA, Scheer WD, Herrera RJ, Deininger PL (1994) African origin of human-specific polymorphic Alu insertions. Proc Natl Acad Sci USA 91:12288–12292Google Scholar
  7. Batzer MA, Rubin CM, Hellman-Blumberg U, Alegria-Hartman M, Leeflang EP, Stern JD, Bazan HA, Shaikh TH, Deininger PL, Schmid CW (1995) Dispersion and insertion polymorphism in two small subfamilies of recently amplified human Alu repeats. J Mol Biol 247:418–427Google Scholar
  8. Batzer MA, Alegria-Hartman M, Bazan H, Kass DH, Shaikh TH, Novick GE, Ioannou PA, Boudreau DA, Scheer WD, Herrera RJ, Stoneking M, Deininger PL (1993) Alu repeats as markers for human population genetics. In: Proceedings of the fourth international symposium on human identification. Promega Publishing, Madison, WI, pp 49–57Google Scholar
  9. Bowcock AM, Bucci C, Hebert JM, Kidd JR, Kidd KK, Friedlaender IS, Cavalli-Sforza, LL (1987) Study of 47 DNA markers in five populations from four continents. Gene Geography 1:47–64Google Scholar
  10. Bowcock AM, Kidd JR, Mountain JL, Hebert JM, Carotenuto L, Kidd KK, Cavalli-Sforza, LL (1991) Drift, admixture, and selection in human evolution: a study with DNA polymorphisms. Proc Natl Acad Sci USA 88:839–843Google Scholar
  11. Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457Google Scholar
  12. Britten RJ, Baron WF, Stout DB, Davidson EH (1988) Sources and evolution of human Alu repeated sequences. Proc Natl Acad Sci USA 85:4770–4774Google Scholar
  13. Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature 325:31–36Google Scholar
  14. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32:550–570Google Scholar
  15. Cavalli-Sforza LL, Piazza A, Menozzi P, Mountain J (1988) Reconstruction of human evolution: bringing together genetic, archaeological, and linguistic data. Proc Natl Acad Sci USA 85:6002–6006Google Scholar
  16. Cavalli-Sforza LL, Menozzi P, Piazza A (1993) Demic expansions and human evolution. Science 259:639–646Google Scholar
  17. Chakraborty R, Kamboh MI, Nwankwo M, Ferrell RE (1992) Caucasian genes in American blacks: new data. Am J Hum Genet 50: 145–155Google Scholar
  18. Deininger PL (1989) SINEs: short interspersed repeated DNA elements in higher eucaryotes. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, DC, pp 619–636Google Scholar
  19. Deininger PL, Batzer MA (1993) Evolution of Retroposons. Evol Biol 27:157–196Google Scholar
  20. Deininger PL, Batzer MA (1995) SINE master genes and population biology. In: Maraia RJ (ed) The impact of short interspersed elements (SINEs) on the host genome. RG Landes, Georgetown, TX, pp 43–60Google Scholar
  21. Deininger PL, Slagel VK (1988) Recently amplified Alu family members share a common parental Alu sequence. Mol Cell Biol 8:4566–4569Google Scholar
  22. Deininger PL, Batzer MA, Hutchison III CA, Edgell MH (1992) Master genes in mammalian repetitive DNA amplification. Trends Genet 8:307–311Google Scholar
  23. DiRienzo A, Wilson AC (1991) Branching pattern in the evolutionary tree for human mitochondrial DNA. Proc Natl Acad Sci USA 88: 1597–1601Google Scholar
  24. Edwards MC, Gibbs RA (1992) A human dimorphism resulting from loss of an Alu. Genomics 14:590–597Google Scholar
  25. Felsenstein J (1981) Evolutionary trees from gene frequencies and quantitative characters: finding maximum likelihood estimates. Evolution 35:1229–1242Google Scholar
  26. Hammer MF (1994) A recent insertion of an Alu element on the Y chromosome is a useful marker for human population studies. Mol Biol Evol 11:749–761Google Scholar
  27. Harpending HC, Ward RH (1982) Chemical systematics and human populations. In: Nitecki M (ed) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp 213–256Google Scholar
  28. Hutchinson GB, Andrew SE, McDonald H, Goldberg YP, Graham R, Rommens JR, Hayden MR (1993) An Alu element retroposition in two families with Huntington disease defines a new active Alu subfamily. Nucleic Acids Res 21:3379–3383Google Scholar
  29. Jurka J (1993) A new subfamily of recently retroposed Alit repeats. Nucleic Acids Res 21:2252Google Scholar
  30. Jurka J, Milosavljevic A (1991) Reconstruction and analysis of human Alu genes. J Mal Evol 32:105–121Google Scholar
  31. Jurka J, Smith T (1988) A fundamental division in the Alu family of repeated sequences. Proc Natl Acad Sci USA 85:4775–4778Google Scholar
  32. Karathanasis SK (1985) Apolipoprotein multigene family: tandem organization of apolipoprotein AI, CIII, and AIV genes. Proc Natl Acad Sci USA 82:6374–6378Google Scholar
  33. Kass DH, Batzer MA, Deininger PL (1995) Gene conversion as a secondary mechanism of SINE evolution. Mol Cell Biol 15:19–25Google Scholar
  34. Kass DH, Aleman C, Batzer MA, Deininger PL (1994) Identification of a human specific Alu insertion in the Factor XIIIB gene. Genetica 94:1–8Google Scholar
  35. Leeflang EP, Liu W-M, Hashimoto C, Choudary PV, Schmid CW (1992) Phylogenetic evidence for multiple Alu source genes. J Mol Evol 35:7–16Google Scholar
  36. Leeflang EP, Liu WM, Chesnokov IN, Schmid CW (1993) Phylogenetic isolation of a human Alu founder gene: drift to new subfamily identity. J Mol Evol 37:559–565Google Scholar
  37. Matera AG, Hellmann U, Schmid CW (1990a) A transpositionally and transcriptionally competent Alu subfamily. Mol Cell Biol 10:5424–5432Google Scholar
  38. Matera AG, Hellmann U, Hintz MF, Schmid CW (1990b) Recently transposed Alu repeats result from multiple source genes. Nucleic Acids Res 18:6019–6023Google Scholar
  39. Merriweather DA, Clark AG, Ballinger SW, Schurr TG, Soodyall H, Jenkins T, Sherry S T, Wallace DW (1991) The structure of human mitochondrial DNA variation. J Mol Evol 33:543–555Google Scholar
  40. Monson KL, Moisan JP, Pascal O, McSween M, Aubert D, Giusti A, Budowle B, Lavergne L (in press) Description and analysis of alleles distribution for four VNTR markers in French and French Canadian populations. Hum HeredGoogle Scholar
  41. Muratani K, Hada T, Yamamoto Y, Kaneko T, Shigeto Y, Ohue T, Furuyama J, Higashino K (1991) Inactivation of the cholinesterase gene by Alu insertion: possible mechanism for human gene transposition. Proc Natl Acad Sci USA 88:11315–11319Google Scholar
  42. Nei M (1972) Genetic distance between populations. Am Naturalist 106:283–292Google Scholar
  43. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  44. Nei M, Roychoudhury AK (1993) Evolutionary relationships of human populations on a global scale. Mol Biol Evol 10:927–943Google Scholar
  45. Okada N (1991) SINEs. Curr Opin Genet Dev 1:498–504Google Scholar
  46. Perna NT, Batzer MA, Deininger PL, Stoneking M (1992) Alu insertion polymorphism: A new type of marker for human population studies. Hum Biol 64:641–648Google Scholar
  47. Piazza A (1993) Who are the Europeans? Science 260:1767–1769Google Scholar
  48. Quentin Y (1988) The Alu family developed through successive waves of fixation closely connected with primate lineage history. J Mol Evol 27:194–202Google Scholar
  49. Reynolds JB, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105:767–779Google Scholar
  50. Rogers J (1983) Retroposons defined. Nature 301:460Google Scholar
  51. Sawada I, Schmid CW (1986) Primate evolution of the α-globin gene cluster and its Alu-like repeats. J Mol Biol 192:693–703Google Scholar
  52. Sawada I, Willard C, Shen C-KJ, Chapman B, Wilson AC, Schmid CW (1985) Evolution of Alu family repeats since the divergence of human and chimpanzee. J Mol Evol 22:316–322Google Scholar
  53. Schmid CW, Maraia R (1992) Transcriptional regulation and transpositional selection of active SINE sequences. Curr Opin Genet Dev 2:874–882.Google Scholar
  54. Shen M-R, Batzer MA, Deininger PL (1991) Evolution of the master Alu gene(s). J Mot Evol 33:311–320Google Scholar
  55. Slagel V, Flemington E, Traina-Dorge V, Bradshaw H, Deininger PL (1987) Clustering and sub-family relationships of the Alu family in the human genome. Mol Biol Evol 14:19–29Google Scholar
  56. Tiret L, Riget B, Visvikis S, Breda C, Corvol P, Cambien F, Soubrier F (1992) 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 51:197–205Google Scholar
  57. Torroni A, Lott MT, Cabell MF, Chen Y-S, Lavergne L, Wallace DC (1994) mtDNA and the origin of Caucasians: identification of ancient Caucasian-specific haplogroups, one of which is prone to a recurrent somatic duplication in the D-loop region. Am J Hum Genet 55:760–776Google Scholar
  58. Ullu E, Murphy S, Melli M (1982) Human 7S RNA consists of a 140 nucleotide middle repetitive sequence inserted in an Alu sequence. Cell 29:195–202Google Scholar
  59. Vidaud D, Vidaud M, Bahnak BR, Siguret V, Sanchez SG, Laurin Y, Meyer D, Goossens M, Lavergne JM (1993) Hemophilia B due to a de novo insertion of a Human-Specific Alu subfamily member within the coding region of the factor IX gene. Fur J Hum Genet 1:30–36Google Scholar
  60. Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC (1991) African populations and the evolution of human mitochondrial DNA. Science 253:1503–1507Google Scholar
  61. Wainscoat JS, Hill AVS, Boyce AL, Flint J, Hernandez M, Thein SL, Old JM, Lynch JR, Falusi AG, Weatherall DJ, Clegg JB (1986) Evolutionary relationships of human populations from an analysis of nuclear DNA polymorphisms. Nature 319:491–493Google Scholar
  62. Wallace MR, Andersen LB, Saulino AM, Gregory PE, Glover TW, Collins FS (1991) A de novo Alu insertion results in neurofibromatosis type 1. Nature 353:864–866Google Scholar
  63. Webb GC, Coggan M, Ichinose A, Board PG (1989) Localization of the coagulation factor XIII B subunit gene (F13B) to chromosome bands 1q31–32.1 and restriction fragment polymorphism at the locus. Hum Genet 81:157–160Google Scholar
  64. Willard C, Nguyen HT, Schmid CW (1987) Existence of at least three distinct Alu subfamilies. J Mol Evol 26:180–186Google Scholar
  65. Yang-Feng TL, Opdenakker G, Volckaert G, Franke U (1986) Human tissue-type plasminogen activator gene located near chromosomal breakpoint in myeloproliferative disorder. Am J Hum Genet 39: 79–87Google Scholar
  66. Zietkiewicz E, Richer C, Makalowski W, Jurka J, Labuda D (1994) A young Alu subfamily amplified independently in human and African great apes lineages. Nucleic Acids Res 22:5608–5612Google Scholar

Copyright information

© Springer-Verlag New York Inc 1996

Authors and Affiliations

  • Mark A. Batzer
    • 1
  • Santosh S. Arcot
    • 1
  • Joshua W. Phinney
    • 1
  • Michelle Alegria-Hartman
    • 1
  • David H. Kass
    • 2
  • Stephen M. Milligan
    • 3
  • Colin Kimpton
    • 4
  • Peter Gill
    • 4
  • Manfred Hochmeister
    • 5
  • Panayiotis A. Ioannou
    • 6
  • Rene J. Herrera
    • 7
  • Donald A. Boudreau
    • 8
  • W. Douglas Scheer
    • 8
  • Bronya J. B. Keats
    • 9
  • Prescott L. Deininger
    • 2
    • 10
  • Mark Stoneking
    • 11
  1. 1.Human Genome Center, L-452, Biology and Biotechnology Research ProgramLawrence Livermore National LaboratoryCALivermoreUSA
  2. 2.Department of Biochemistry and Molecular Biology, Center for Human and Molecular GeneticsLouisiana State University Medical CenterNew OrleansUSA
  3. 3.DNA UnitMichigan State PoliceEast LansingUSA
  4. 4.Forensic Science ServiceBirminghamUK
  5. 5.Department of Forensic MedicineUniversity of BernBernSwitzerland
  6. 6.The Cyprus Institute of Neurology and GeneticsNicosiaCyprus
  7. 7.Department of Biological Sciences, Florida International UniversityUniversity Park CampusMiamiUSA
  8. 8.Department of PathologyLouisiana State University Medical CenterNew OrleansUSA
  9. 9.Department of Biometry and Genetics, Center for Human and Molecular GeneticsLouisiana State University Medical CenterNew OrleansUSA
  10. 10.Laboratory of Molecular GeneticsAlton Ochsner Medical FoundationNew OrleansUSA
  11. 11.Department of AnthropologyPennsylvania State UniversityUniversity ParkUSA

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