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Retroposon Mapping in Molecular Systematics

  • Norihiro Okada
  • Andrew M. Shedlock
  • Masato Nikaido
Part of the Methods in Molecular Biology book series (MIMB, volume 260)

Abstract

Advances in genome sciences are demonstrating the dynamic nature of noncoding DNA regions, which are comprised largely of repetitive elements with no apparent function. Retroposons are one class of mobile genetic elements that amplify and move about the genome via a copy-and-paste mechanism that employs an RNA intermediate. Short and long interspersed elements (SINEs and LINEs, respectively) are types of retroposons of particular interest because of their active role in shaping the architecture of genomes and their diagnostic value as evolutionary markers for studies of phylogeny and population biology. Although the use of SINEs and LINEs for molecular systematic studies is proliferating, a comprehensive laboratory protocol that explicitly outlines how to isolate and characterize retroposons for systematic studies in a detailed, step-by-step fashion has been lacking. The present chapter addresses this gap in the literature by focusing on the strategy for isolating new SINEs from a genomic library, the screening process, the sequencing and characterization of clones into subfamilies, quantification of copy number in host taxa, and the critical diagnosis of phylogenetically informative SINE and LINE insertion patterns. Practical limits to the method are discussed in relation to sampling design, systematic character theory, and the empirical distribution of elements observed in eukaryotic lineages. Major steps in the experimental process are illustrated with case examples from a diversity of taxonomic groups and by published results in the molecular biology and systematics literature.

Key Words

DNA repeat mobile DNA interspersed element retroposon SINE LINE retrotransposition reverse transcriptase cDNA RNA systematics genomics eukaryote 

References

  1. 1.
    Kazazian, H. H., Jr., and Moran, J. V. (1998) The impact of L1 retrotransposons on the human genome. Nature Genet. 19, 19–24.PubMedCrossRefGoogle Scholar
  2. 2.
    Brosius, J. (1991) Retroposons—seeds of evolution. Science 251, 753.PubMedCrossRefGoogle Scholar
  3. 3.
    Shedlock, A. M. and Okada, N. (2000) SINE insertions: Powerful tools for molecular systematics. BioEssays 22, 148–160.PubMedCrossRefGoogle Scholar
  4. 4.
    Rogers, J. (1983) Retroposons defined. Nature 301, 460.PubMedCrossRefGoogle Scholar
  5. 5.
    Weiner, A., Deininger, P. L., and Efstratiadis, A. (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu. Rev. Biochem. 55, 631–661.PubMedCrossRefGoogle Scholar
  6. 6.
    Schmid, C. (1996) Alu: structure, origin, evolution, significance and function of one-tenth of human DNA. Prog. Nucl. Acid Res. and Mol. Biol. 53, 283–319.CrossRefGoogle Scholar
  7. 7.
    Clark, J. B. and Kidwell, M. (1997) A phylogenetic perspective on P transposable element evolution in Drosophila. Proc. Natl. Acad. Sci. USA 94, 11,428–11,433.PubMedCrossRefGoogle Scholar
  8. 8.
    Hartl, D. L., Lohe, A. R., and Lozovskya, E. R. (1997) Modern thoughts on an ancient mariner: function, evolution, regulation. Annu. Rev. Genet. 31, 337–358.PubMedCrossRefGoogle Scholar
  9. 9.
    Okada, N. (1991) SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol. Evol. 6, 358–361.PubMedCrossRefGoogle Scholar
  10. 10.
    Okada, N. (1991) SINEs. Curr. Opin. Genet. Dev. 1, 498–504.PubMedCrossRefGoogle Scholar
  11. 11.
    Eickbush, T. H. Origin and evolutionary relationships of retroelements. In The Evolutionary Biology of Viruses (Morse, S. S., ed.), Raven, New York, NY, 1994, pp. 121–157.Google Scholar
  12. 12.
    Nishihara, H., Terai, Y., and Okada, N. (2002) Characterization of novel Alu-and tRNA-related SINEs from the tree shrew and evolutionary implications of their origins. Mol. Biol. Evol. 19, 1964–1972.PubMedGoogle Scholar
  13. 13.
    Ohshima, K., Hamada, M., Terai, Y., and Okada, N. (1996) The 3′ ends of tRNA-derived short interspersed repetitive elements are derived from the 3′ ends of long interspersed repetitive elements. Mol. Cell. Biol. 16, 3756–3764.PubMedGoogle Scholar
  14. 14.
    Okada, N. and Ohshima, K. Evolution of tRNA-derived SINEs. In The Impact of Short Interspersed Elements (SINEs) on the Host Genome (Maraia, R. J., ed.), RG Landes Co., Austin, TX, 1995, pp. 62–79.Google Scholar
  15. 15.
    Okada, N., Hamada, M., Ogiwara, I., and Ohshima, K. (1997) SINEs and LINEs share common 3′ sequences: a review. Gene 205, 229–243.PubMedCrossRefGoogle Scholar
  16. 16.
    Terai, Y., Takahashi, K., and Okada, N. (1998) SINE Cousins: The 3′ end tails of the two oldest and distantly related families of SINEs are descended from the 3′ ends of LINEs with the same genealogical origin. Mol. Biol. Evol. 15, 1460–1471.PubMedGoogle Scholar
  17. 17.
    Kajikawa, M. and Okada, N. (2002) LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 111, 433–444.PubMedCrossRefGoogle Scholar
  18. 18.
    Murata, S., Takasaki, N., Saitoh, M., and Okada, N. (1993) Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. Proc. Natl. Acad. Sci. USA 90, 6995–6999.PubMedCrossRefGoogle Scholar
  19. 19.
    Shimamura, M., Yasue, H., Ohshima, K., Abe, H., Kato, H., Kishiro, T., et al. (1997) Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 388, 666–670.PubMedCrossRefGoogle Scholar
  20. 20.
    Takahashi, K., Terai, Y., Nishida, M., and Okada, N. (1998) A novel family of short interspersed repetitive elements (SINEs) from cichlids: the pattern of insertion of SINEs at orthologous loci support the proposed monophyly of four major groups of cichlid fishes in Lake Tanganyika. Mol. Biol. Evol. 15, 391–407.PubMedGoogle Scholar
  21. 21.
    Nikaido, M., Rooney, A. P., and Okada, N. (1999) Phylogenetic relationships among cetartiodactyls based on insertions of short and long interspersed elements: Hippopotamuses are the closest extant relatives of whales. Proc. Natl. Acad. Sci. USA 96, 10,261–10,266.PubMedCrossRefGoogle Scholar
  22. 22.
    Deininger, P. L. and Batzer, M. A. (1993) Evolution of retroposons. Evol. Biol. 27, 157–196.Google Scholar
  23. 23.
    Rokas, A. and Holland, P. W. (2000) Rare molecular changes as a tool for phylogenetics. Trends Ecol. Evol. 15, 454–459.PubMedCrossRefGoogle Scholar
  24. 24.
    Shedlock, A. M., Milinkovitch, M. C., and Okada, N. (2000) SINE evolution, missing data, and the origin of whales. Syst. Biol. 49, 808–817.PubMedCrossRefGoogle Scholar
  25. 25.
    Hillis, D. M. (1999) SINEs of the perfect character. Proc. Natl. Acad. Sci. USA 96, 9979–9981.PubMedCrossRefGoogle Scholar
  26. 26.
    Miyamoto, M. M. (2000) Perfect SINEs of evolutionary history? Current Biology 9, 816–819.CrossRefGoogle Scholar
  27. 27.
    Schmid, C. W. and Maraia, R. (1992) Transcriptional regulation and transpositional selection of active SINE sequences. Curr. Opin. Genet. Devel. 2, 874–882.CrossRefGoogle Scholar
  28. 28.
    Kim, J., Martignetti, J. A., Shen, M. R., Brosius, J., and Deininger, P. (1994) Rodent BC1 RNA gene as a master gene for ID element amplification. Proc. Natl. Acad. Sci. USA 91, 3607–3611.PubMedCrossRefGoogle Scholar
  29. 29.
    Shen, M. R., Batzer, M. A., and Deininger, P. L. (1991) Evolution of the Master Alu Gene(s). J. Mol. Evol. 33, 311–320.PubMedCrossRefGoogle Scholar
  30. 30.
    Matera, A. G., Hellman, U., and Schmid, C. W. (1990) A transpositionally and transcriptionally competent Alu subfamily. Mol. Cell. Biol. 10, 5424–5432.PubMedGoogle Scholar
  31. 31.
    Leeflang, E. P., Liu, W. M., Hashimoto, C., Choudary, P. V., and Schmid, C. W. (1992) Phylogenetic evidence for multiple Alu source genes. J. Mol. Evol. 35, 7–16.PubMedCrossRefGoogle Scholar
  32. 32.
    Kido, Y., Himberg, M., Takasaki, N., and Okada, N. (1994) Amplification of distinct subfamilies of short interspersed elements (SINEs) during evolution of the Salmonidae. J. Mol. Biol. 241, 633–644.PubMedCrossRefGoogle Scholar
  33. 33.
    Takasaki, N., Murata, S., Saitoh, M., Kobayashi, T., Park, L., and Okada, N. (1994) Species-specific amplification of tRNA-derived short interspersed repetitive elements (SINEs) by retroposition: A process of parasitization of entire genomes during the evolution of salmonids. Proc. Natl. Acad. Sci. USA 91, 10,153–10,157.PubMedCrossRefGoogle Scholar
  34. 34.
    Hennig, W. (ed.) Phylogenetic Systematics. University of Illinois Press, Urbana-Champagne, IL, 1996.Google Scholar
  35. 35.
    Hendy, M. D. and Penny, D. (1989) A framework for the quantitative study of evolutionary trees. Syst. Zool. 38, 297–309.CrossRefGoogle Scholar
  36. 36.
    Nei, M. and Kumar, S. (eds.) Molecular Evolution and Phylogenetics. Oxford University Press, New York, NY, 2000.Google Scholar
  37. 37.
    Manley, J. L., Fire, A., Cano, A., Sharp, P. A., and Gefter, M. L. (1980) DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc. Natl. Acad. Sci. USA 83, 3156–3160.Google Scholar
  38. 38.
    Talkington, C. A., Nishioka, Y., and Leder, P. (1980) In vitro transcription of normal, mutant, and truncated mouse α-globin genes. Proc. Natl. Acad. Sci. USA 77, 7132–7136.PubMedCrossRefGoogle Scholar
  39. 39.
    Blin, N. and Stafford, D. W. (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 13, 537–556.Google Scholar
  40. 40.
    Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403–410.PubMedGoogle Scholar
  41. 41.
    Sherry, S. T., Harpending, H. C., Batzer, M. A., and Stoneking, M. (1997) Alu evolution in human populations: Using the coalescent to estimate effective population size. Genetics 147, 1977–1982.PubMedGoogle Scholar
  42. 42.
    Endoh, H. and Okada, N. (1986) Total DNA transcription in vitro: a procedure to detect highly repetitive and transcribable sequences with tRNA-like structures. Proc. Natl. Acad. Sci. USA 83, 251–255.PubMedCrossRefGoogle Scholar
  43. 43.
    Matsumoto, K., Murakami, K., and Okada, N. (1986) Gene for lysine tRNA1 may be a progenitor of the highly repetitive and transcribable sequences present in the salmon genome. Proc. Natl. Acad. Sci. USA 83, 3156–3160.PubMedCrossRefGoogle Scholar
  44. 44.
    Nikaido, M., Nishihara, H., Fukumoto, Y., and Okada, N. (2003) Ancient SINEs from African Endemic Mammals. Mol. Biol. Evol. 20, 522–527.PubMedCrossRefGoogle Scholar
  45. 45.
    Sprinzl, M., Hartmann, T., Meissner, F., Moll, J., and Vorderwülbecke, T. (1987) Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 15, r53–r188.PubMedGoogle Scholar
  46. 46.
    Galli, G., Hofstetter, H., and Birnstiel, M. L. (1981) Two conserved sequence blocks within eukaryotic tRNA genes are major promoter elements. Nature 294, 626–631.PubMedCrossRefGoogle Scholar
  47. 47.
    Smit, A. F. A., Toth, G., Riggs, A. D., and Jurka, J. (1995) Ancestral, mammalianwide subfamilies of LINE-1 repetitive sequences. J. Mol. Evol. 246, 401–417.Google Scholar
  48. 48.
    Britten, R. J., Baron, W. F., Stout, D. B., and Davidson, E. H. (1988) Sources and evolution of human Alu repeated sequences. Proc. Natl. Acad. Sci. USA 85, 4770–4774.PubMedCrossRefGoogle Scholar
  49. 49.
    Jurka, J., Zeitkiewicz, E., and Labuda, D. (1995) Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the Mesozonic era. Nucleic Acids Res. 23, 170–175.PubMedCrossRefGoogle Scholar
  50. 50.
    Nikaido, M., Matsuno, F., Abe, H., Shimamura, M., Matsubayashi, H., and Okada, N. (2001) Evolution of CHR-2 SINEs in cetartiodactyl genomes: possible evidence for the monophyletic origin of toothed whales. Mamm. Genome 12, 909–915.PubMedCrossRefGoogle Scholar
  51. 51.
    Nikaido, M., Matsuno, F., Hamilton, H., Brownell, R. L., Jr., Cao, Y., Wang, D., et al. (2001) Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc. Natl. Acad. Sci. USA 98, 7384–7389.PubMedCrossRefGoogle Scholar
  52. 52.
    Waddel, P. J., Okada, N., and Hasegawa, M. (1999) Towards resolving the interordinal relationships of placental mammals. Syst. Biol. 48, 1–5.CrossRefGoogle Scholar
  53. 53.
    Cao, Y., Fujiwara, M., Nikaido, M., Okada, N., and Hasegawa, M. (2000) Interordinal relationships and timescale of eutherian evolution as inferred from mitochondrial genome data. Gene 259, 149–158.PubMedCrossRefGoogle Scholar
  54. 54.
    Nikaido, M., Harada, M., Cao, Y., Hasegawa, M., and Okada, N. (2000) Monophyletic origin of the order Chiroptera and its phylogenetic position among mammalia, as inferred from the complete sequence of the mitochondrial DNA of a Japanese megabat, the Ryukyu flying fox (Pteropus dasymallus). J. Mol. Evol. 51, 318–328.PubMedGoogle Scholar
  55. 55.
    Nikaido, M., Kawai, K., Cao, Y., Harada, M., Okada, N., and Hasegawa, M. (2001) Maximum likelihood analysis of the complete mitochondrial genomes of eutherians and a reevaluation of the phylogeny of bats and insectivores. J. Mol. Evol. 53, 508–516.PubMedCrossRefGoogle Scholar
  56. 56.
    Smit, A. F. A. and Riggs, A. D. (1995) MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation. Nucleic Acids Res. 23, 98–102.PubMedCrossRefGoogle Scholar
  57. 57.
    Piscurek, O., Nikaido, M., Boeadi, M., and Okada, N. (2003) Unique mammalian tRNA-derived repetitive elements in Dermopterans: the t-SINE family and its retrotransposon through multiple sources. Mol. Biol. Evol. 20, 1659–1668.CrossRefGoogle Scholar
  58. 58.
    Shimamura, M., Abe, H., Nikaido, M., Ohshima, K., and Okada, N. (1999) Genealogy of families of SINEs in cetacean and artiodactyls: The presence of a huge superfamily of tRNAGlu-derived families of SINEs. Mol. Biol. Evol. 16, 1046–1060.PubMedGoogle Scholar
  59. 59.
    Minnick, M. F., Stillwell, L. C., Heineman, J. M., and Stiegler, G. L. (1992) A highly repetitive DNA sequence possibly unique to canids. Gene 110, 235–238.PubMedCrossRefGoogle Scholar
  60. 60.
    Coltman, D. W. and Wright, J. M. (1994) Can SINEs: a family of tRNA-derived retroposons specific to the superfamily Canoidea. Nucleic Acids Res. 22, 2726–2730.PubMedCrossRefGoogle Scholar
  61. 61.
    van der Vlugt, H. H. J. and Lenstra, J. A. (1995) SINE elements of carnivores. Mamm. Genome 6, 49–51.PubMedCrossRefGoogle Scholar
  62. 62.
    Sakagami, M., Ohshima, K., Mukoyama, H., Yasue, H., and Okada, N. (1994) A novel tRNA species as an origin of short interspersed repetitive elements (SINEs). Equine SINEs may have originated from tRNA(Ser). J. Mol. Biol. 239, 731–735.PubMedCrossRefGoogle Scholar
  63. 63.
    Gallagher, P. C., Lear, T. L., Coogle, L. D., and Bailey, E. (1999) Two SINE families associated with equine microsatellite loci. Mamm. Genome 10, 140–144.PubMedCrossRefGoogle Scholar
  64. 64.
    Borodulina, O. R. and Kramerov, D. A. (1999) Wide distribution of short interspersed elements among eukaryotic genomes. FEBS Lett. 457, 409–413.PubMedCrossRefGoogle Scholar
  65. 65.
    Borodulina, O. R. and Kramerov, D. A. (2001) Short interspersed elements (SINEs) from insectivores. Two classes of mammalian SINEs distinguished by A-rich tail structure. Mamm. Genome 10, 779–786.CrossRefGoogle Scholar
  66. 66.
    Schmitz, J., Ohme, M., and Zischler, H. (2001) SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other Primates. Genetics 157, 777–784.PubMedGoogle Scholar
  67. 67.
    Kramerov, D., Vassetzky, N., and Serdobova, I. (1999) The evolutionary position of dormice (Gliridae) in Rodentia determined by a novel short retroposon. Mol. Biol. Evol. 16, 715–717.PubMedGoogle Scholar
  68. 68.
    Kass, D. H., Raynor M. E., and Williams, T. M. (2000) Evolutionary history of B1 retroposons in the genus Mus. J. Mol. Evol. 51, 256–264.PubMedGoogle Scholar
  69. 69.
    Kido, Y., Aono, M., Yamaki, T., Matsumoto, K., Murata, S., Saneyoshi, M., et al. (1991) Shaping and reshaping of salmonid genomes by amplification of tRNAderived retroposon during evolution. Proc. Natl. Acad. Sci. USA 88, 2326–2330.PubMedCrossRefGoogle Scholar
  70. 70.
    Murata, S., Takasaki, N., Saitoh, M., Tachida, H., and Okada, N. (1996) Details of retropositional genome dynamics that provide a rationale for a genetic division: the distinct branching of all the Pacific salmon and trout (Oncorhynchus) from the Atlantic salmon and trout (Salmo). Genetics 142, 915–926.PubMedGoogle Scholar
  71. 71.
    Kido, Y., Saitoh, M., Murata, S., and Okada, N. (1995) Evolution of the active sequences of the HpaI short interspersed elements. J. Mol. Evol. 41, 986–995.PubMedCrossRefGoogle Scholar
  72. 72.
    Takasaki, N., Park, L., Kaeriyama, M., Gharrett, A. J., and Okada, N. (1996) Characterization of species-specifically amplified SINEs in three salmonid species—chum salmon, pink salmon, and kokanee: the local environment of the genome may be important for the generation of a dominant source gene at a newly retroposed locus. J. Mol. Evol. 42, 103–106.PubMedCrossRefGoogle Scholar
  73. 73.
    Izsvak, Z., Ivics, Z., Garcia-Estefania, D., Fahrenkrug, S. C., and Hackett, P. B. (1996) DANA elements: a family of composite, tRNA-derived short interspersed DNA elements associated with mutational activities in zebrafish (Danio rerio). Proc. Natl. Acad. Sci. USA 93, 1077–1081.PubMedCrossRefGoogle Scholar
  74. 74.
    Takahashi, K., Nishida, M., Yuma, M., and Okada, N. (2001) Retroposition of the AFC family of SINEs (Short Interspersed Repetitive Elements) before and during the adaptive radiation of cichlid fishes in lake Malawi and related inferences about phylogeny. J. Mol. Evol. 53, 496–507.PubMedCrossRefGoogle Scholar
  75. 75.
    Ogiwara, I., Miya, M., Ohshima, K., and Okada, N. (2002) V-SINEs: a new superfamily of vertebrate SINEs that are widespread in vertebrate genomes and retain a strongly conserved segment within each repetitive unit. Genome Res. 12, 316–324.PubMedCrossRefGoogle Scholar
  76. 76.
    Nagahashi, S., Endoh, H., Suzuki, Y., and Okada, N. (1991) Characterization of a tandemly repeated DNA sequence family originally derived by retroposition of tRNA(Glu) in the newt. J. Mol. Biol. 222, 391–404.PubMedCrossRefGoogle Scholar
  77. 77.
    Unsal, K. and Morgan, G. T. (1995) A novel group of families of short interspersed repetitive elements (SINEs) in Xenopus: evidence of a specific target site for DNA-mediated transposition of inverted-repeat SINEs. J. Mol. Biol. 248, 812–823.PubMedCrossRefGoogle Scholar
  78. 78.
    Ohshima, K., Koishi, R., Matsuo, M., and Okada, N. (1993) Several short interspersed repetitive elements (SINEs) in distant species may have originated from a common ancestral retrovirus: characterization of a squid SINE and a possible mechanism for generation of tRNA-derived retroposons. Proc. Natl. Acad. Sci. USA 90, 6260–6264.PubMedCrossRefGoogle Scholar
  79. 79.
    Ohshima, K. and Okada, N. (1994) Generality of the tRNA origin of short interspersed repetitive elements (SINEs). Characterization of three different tRNA-derived retroposons in the octopus. J. Mol. Biol. 243, 25–37.PubMedCrossRefGoogle Scholar
  80. 80.
    Mochizuki, K., Umeda, M., Ohtsubo, H., and Ohtsubo, E. (1992) Characterization of a plant SINE, p-SINE1, in rice genomes. Jpn. J. Genet. 67, 155–166.PubMedCrossRefGoogle Scholar
  81. 81.
    Deragon, J. M., Landry, B. S., Pelissier, T., Tutois, S., Tourmente, S., and Picard, G. (1994) An analysis of retroposition in plants based on a family of SINEs from Brassica napus. J. Mol. Evol. 39, 378–386.PubMedCrossRefGoogle Scholar
  82. 82.
    Yoshioka, Y., Matsumoto, S., Kojima, S., Ohshima, K., Okada, N., and Machida, Y. (1993) Molecular characterization of a short interspersed repetitive element from tobacco that exhibits sequence homology to specific tRNAs. Proc. Natl. Acad. Sci. USA 90, 6562–6566.PubMedCrossRefGoogle Scholar
  83. 83.
    Surzycki, S. A. and Belknap, W. R. (1999) Characterization of repetitive DNA elements in Arabidopsis. J. Mol. Biol. 48, 684–691.Google Scholar
  84. 84.
    Hamada, M., Takasaki, N., Reist, J. D., DeCicco, A. L., Goto, A., and Okada, N. (1998) Detection of the ongoing sorting of ancestrally polymorphic SINEs toward fixation or loss in populations of two species of charr during speciation. Genetics 150, 301–311.PubMedGoogle Scholar
  85. 85.
    Takahashi, K., Terai, Y., Nishida, M., and Okada, N. (2001) Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol. Biol. Evol. 18, 2057–2066.PubMedGoogle Scholar
  86. 86.
    Terai, Y., Takahashi, K., Nishida, M., Sato, T., and Okada, N. (2003) Using SINEs to probe ancient explosive speciation: “Hidden” radiation of African Cichlids? Mol. Biol. Evol. 20, 924–930.PubMedCrossRefGoogle Scholar
  87. 87.
    Stoneking, M., Fontius, J. J., Clifford, S. L., Soodyall, H., Arcot, S. S., Saha, N., et al. (1997) Alu insertion polymorphisms and human evolution: Evidence for a larger population size in Africa. Genome Res. 7, 1061–1071.PubMedCrossRefGoogle Scholar
  88. 88.
    Lum, J. K., Nikaido, M., Shimamura, M., Shimodaira, H., Shedlock, A. M., Okada, N., et al. (2000) Consistency of SINE insertion topology and flanking sequence tree: Quantifying relationships among cetartiodactyls. Mol. Biol. Evol. 17, 1417–1424.PubMedGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2004

Authors and Affiliations

  • Norihiro Okada
    • 1
  • Andrew M. Shedlock
    • 2
  • Masato Nikaido
    • 1
  1. 1.Faculty of Bioscience and BiotechnologyTokyo Institute of TechnologyYokohamaJapan
  2. 2.Department of ZoologyUniversity of WashingtonSeattle

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