Skip to main content
SpringerLink
Log in

Large Tandem, Higher Order Repeats and Regularly Dispersed Repeat Units Contribute Substantially to Divergence Between Human and Chimpanzee Y Chromosomes

Journal of Molecular Evolution Aims and scope Submit manuscript

Cite this article

Abstract

Comparison of human and chimpanzee genomes has received much attention, because of paramount role for understanding evolutionary step distinguishing us from our closest living relative. In order to contribute to insight into Y chromosome evolutionary history, we study and compare tandems, higher order repeats (HORs), and regularly dispersed repeats in human and chimpanzee Y chromosome contigs, using robust Global Repeat Map algorithm. We find a new type of long-range acceleration, human-accelerated HOR regions. In peripheral domains of 35mer human alphoid HORs, we find riddled features with ten additional repeat monomers. In chimpanzee, we identify 30mer alphoid HOR. We construct alphoid HOR schemes showing significant human–chimpanzee difference, revealing rapid evolution after human–chimpanzee separation. We identify and analyze over 20 large repeat units, most of them reported here for the first time as: chimpanzee and human ~1.6 kb 3mer secondary repeat unit (SRU) and ~23.5 kb tertiary repeat unit (~0.55 kb primary repeat unit, PRU); human 10848, 15775, 20309, 60910, and 72140 bp PRUs; human 3mer SRU (~2.4 kb PRU); 715mer and 1123mer SRUs (5mer PRU); chimpanzee 5096, 10762, 10853, 60523 bp PRUs; and chimpanzee 64624 bp SRU (10853 bp PRU). We show that substantial human–chimpanzee differences are concentrated in large repeat structures, at the level of as much as ~70% divergence, sizably exceeding previous numerical estimates for some selected noncoding sequences. Smeared over the whole sequenced assembly (25 Mb) this gives ~14% human–chimpanzee divergence. This is significantly higher estimate of divergence between human and chimpanzee than previous estimates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Alexandrov IA, Kazakov A, Tumeneva I, Shepelev V, Yurov Y (2001) Alpha-satellite DNA of primates: old and new families. Chromosoma 110:253–266

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Hasnian SE (2003) Genomics of the human Y chromosome—1 association with male infertility. Gene 321:25–37

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Archidiacono N, Antonacci R, Marzella R, Finelli P, Lonoce A, Rocchi M (1995) Comparative mapping of human alphoid sequences in great apes using fluorescence in situ hybridization. Genomics 25:477–484

    Article  CAS  PubMed  Google Scholar 

  • Bailey JA, Eichler EE (2006) Primate segmental duplications: crucibles of evolution, diversity and diesease. Nat Rev Genet 7:552–564

    Article  CAS  PubMed  Google Scholar 

  • Baldini A, Miller DA, Miller OJ, Ryder OA, Mitchell AR (1991) A chimpanzee-derived chromosome-specific alpha satellite DNA sequence conserved between chimpanzee and human. Chromosoma 100:156–161

    Article  CAS  PubMed  Google Scholar 

  • Baltimore D (1981) Gene conversion: some implications for immunoglobulin genes. Cell 24:592–594

    Article  CAS  PubMed  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  CAS  PubMed  Google Scholar 

  • Boffelli D, McAuliffe J, Ovcharenko D, Lewis KD, Ovcharenko I, Pachter L, Rubin EM (2003) Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299:1391–1394

    Article  CAS  PubMed  Google Scholar 

  • Britten RJ (2002) Divergence between samples of chimpanzee and human DNA sequences is 5%, counting indels. Proc Natl Acad Sci USA 99:13633–13635

    Article  CAS  PubMed  Google Scholar 

  • Britten RJ, Rowen L, Williams J, Cameron RA (2003) Majority of divergence between closely related DNA samples is due to indels. Proc Natl Acad Sci USA 100:4661–4665

    Article  CAS  PubMed  Google Scholar 

  • Caceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, Geschwind DH, Lockhart DJ, Preuss TM, Barlow C (2003) Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci USA 10:13030–13035

    Article  CAS  Google Scholar 

  • Calos MP, Miller JH (1980) Transposable elements. Cell 20:579–595

    Article  CAS  PubMed  Google Scholar 

  • Carroll SB (2003) Genetics and the making of Homo sapiens. Nature 422:849–857

    Article  CAS  PubMed  Google Scholar 

  • Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68:444–456

    Article  CAS  PubMed  Google Scholar 

  • Cheng Z, Ventura M, She XW, Khaitovich P, Graves T, Osoegawa K, Church D, DeJong P, Wilson RK, Paabo S, Rocchi M, Eichler EE (2005) A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437:88–93

    Article  CAS  PubMed  Google Scholar 

  • Choo KHA (1997) The Centromere. Oxford University Press, Oxford

    Google Scholar 

  • Cooper KF, Fisher RB, Tyler-Smith C (1993a) The major centromeric array of alphoid satellite DNA on the human Y chromosome is non-palindromic. Hum Mol Genet 2:1267–1270

    Article  CAS  PubMed  Google Scholar 

  • Cooper KF, Fisher RB, Tyler-Smith C (1993b) Structure of the sequences adjacent to the centromeric alphoid satellite DNA array on the human Y chromosome. J Mol Biol 230:787–799

    Article  CAS  PubMed  Google Scholar 

  • D’Aiuto L, Antonacci R, Marzella R, Archidiacono N, Rocchi M (1993) Cloning an comparative mapping of a human chromosome 4-specific alpha satellite DNA sequence. Genomics 18:230–235

    Article  PubMed  Google Scholar 

  • de Knijff P (2006) The human Y chromosome is not dead (yet). Heredity 97:377–378

    Article  PubMed  CAS  Google Scholar 

  • Dorit RL, Akashi H, Gilbert W (1995) Absence of polymorphism at the ZFY locus on the human Y chromosome. Science 268:1183–1185

    Article  CAS  PubMed  Google Scholar 

  • Dorus S, Vallender EJ, Evans PD, Anderson JR, Gilbert SL, Mahowald M, Wyckoff GJ, Malcom CM, Lahn BT (2004) Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119(7):1027–1040

    Article  CAS  PubMed  Google Scholar 

  • Dover G (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–116

    Article  CAS  PubMed  Google Scholar 

  • Dover G (1986) Molecular drive in multigene families: how biological novelties arise, spread and are asasimilated. Trends Genet 2:159–165

    Article  CAS  Google Scholar 

  • Durfy SJ, Willard HF (1989) Patterns of intra- and interarray sequence variation in alpha satellite from the human X chromosome: evidence for short-range homogenization of tandemly repeated DNA sequences. Genomics 5:810–821

    Article  CAS  PubMed  Google Scholar 

  • Durfy SJ, Willard HF (1990) Concerted evolution of primate alpha satellite DNA. Evidence for ancestral sequence shared by gorilla and human X chromosome alpha satellite. J Mol Biol 216:555–566

    Article  CAS  PubMed  Google Scholar 

  • Ebersberger I, Metzler D, Schwarz C, Paabo S (2002) Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet 70:1490–1497

    Article  CAS  PubMed  Google Scholar 

  • Ebersberger I, Galgoczy P, Taudien S, Taenzer S, Platzer M, von Haeseler A (2007) Mapping human ancestry. Mol Biol Evol 24:2266–2276

    Article  CAS  PubMed  Google Scholar 

  • Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V, Kitano T, Monaco AP, Paabo S (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869–872

    Article  CAS  PubMed  Google Scholar 

  • Fernandes AT, Fernandes S, Goncalves R, Sa R, Costa P, Rosa A, Ferras C, Sousa M, Brehm A, Barros A (2006) DAZ gene copies: evidence of Y chromosome evolution. Mol Hum Reprod 12:519–523

    Article  CAS  PubMed  Google Scholar 

  • Fujiyama A, Watanabe H, Toyoda A, Taylor TD, Itoh T, Tsai SF, Park HS, Yaspo ML, Lehrach H, Chen Z et al (2002) Construction and analysis of a human–chimpanzee comparative clone-map. Science 295:131–134

    Article  PubMed  Google Scholar 

  • Gelfand Y, Rodriguez A, Benson G (2007) TRDB—the tandem repeats database. Nucleic Acids Res 35:D80–D87

    Article  CAS  PubMed  Google Scholar 

  • Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, Mardis ER, Remington KA, Strausberg RL, Venter JC, Wilson RK et al (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316:222–234

    Article  CAS  PubMed  Google Scholar 

  • Gierer A (1998) Networks of gene regulation, neural development and the evolution of general capabilities, such as human empathy. Z Naturforsch C 53(7–8):716–722

    CAS  PubMed  Google Scholar 

  • Gierer A (2004) Human brain evolution, theories of innovation, and lessons from the history of technology. J Biosci 29:235

    Article  PubMed  Google Scholar 

  • Glaser B, Yen PH, Schempp W (1998) Fibre-fluorescence in situ hybridization unravels apparently seven DAZ genes or pseudogenes clustered within a Y chromosome region frequently deleted in azoospermic males. Chromosome Res l:481–486

    Article  Google Scholar 

  • Glusman G, Sosinsky A, Ben-Asher E, Avidan N, Sonkin D, Bahar A, Rosenthal A, Clifton S, Roe B, Ferraz C, Demaille J, Lancet D (2000) Sequence, structure, and evolution of a complete human olfactory receptor gene cluster. Genomics 63:227–245

    Article  CAS  PubMed  Google Scholar 

  • Graves JA (1995) The origin and function of the mammalian Y chromosome and Y-borne genes - an evolving understanding. Bioessays 17:311–320

    Article  CAS  PubMed  Google Scholar 

  • Haaf T, Willard HF (1992) Organization, polymorphism, and molecular cytogenetics of chromosome-specific alpha-satellite DNA from the centromere of chromosome 2. Genomics 13:122–128

    Article  CAS  PubMed  Google Scholar 

  • Haaf T, Willard HF (1997) Chromosome specific alpha satellite DNA from the centromere of chimpanzee chromosome 4. Chromosoma 106:226–232

    Article  CAS  PubMed  Google Scholar 

  • Haaf T, Willard HF (1998) Orangutan alpha satellite monomers are closely related to the human consensus sequence. Mamm Genome 9:440–447

    Article  CAS  PubMed  Google Scholar 

  • Haaf T, Matera AG, Wienberg J, Ward DC (1995) Presence and abundance of CENP-B box sequences in great ape subsets of primate-specific α-satellite DNA. J Mol Evol 41:487–491

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S (2002) Near the edge of a chromosomes “black hole”. Trends Genet 18:165–167

    Article  CAS  PubMed  Google Scholar 

  • Hourcade D, Dressler D, Wolfson J (1973) The amplification of ribosomal RNA genes involves a rolling circle intermediate. Proc Natl Acad Sci USA 70:2926–2930

    Article  CAS  PubMed  Google Scholar 

  • Hughes JF, Skaletsky H, Pyntikova T, Minx PJ, Graves T, Rozen S, Wilson RK, Page DC (2005) Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee. Nature 437:101–104

    CAS  Google Scholar 

  • Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SKM, Minx PJ, Fulton RS, McGrath SD, Locke DP, Friedman C et al (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539

    Article  CAS  PubMed  Google Scholar 

  • Jobling MA, Tyler-Smith C (2003) The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet 4:598–612

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen AL, Bostock CJ, Bak AL (1986) Chromosome-specific subfamilies within human alphoid repetitive DNA. J Mol Biol 187:185–196

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen AL, Laursen HB, Jones C, Bak AL (1992) Evolutionarily different alphoid repeat DNA on homologous chromosomes in human and chimpanzee. Proc Natl Acad Sci USA 89:3310–3314

    Article  CAS  PubMed  Google Scholar 

  • Kehrer-Sawatzki H, Cooper DN (2007) Structural divergence between the human and chimpanzee genomes. Hum Genet 120:759–778

    Article  CAS  PubMed  Google Scholar 

  • Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M, Franz H, Weiss G, Lachmann M, Paabo S (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309:1850–1854

    Article  CAS  PubMed  Google Scholar 

  • King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116

    Article  CAS  PubMed  Google Scholar 

  • Kirsch S, Muench C, Jiang Z, Cheng Z, Chen L, Batz C, Eichler EE, Schempp W (2008) Evolutionary dynamics of segmental duplications from human Y-chromosomal euchromatin/heterochromatin transition regions. Genome Res 18:1030–1042

    Article  CAS  PubMed  Google Scholar 

  • Krystal M, D′Eustachio P, Ruddle FH, Arnheim N (1981) Human nucleolus organizers on non-homologous chromosomes can share the same ribosomal gene variants. Proc Natl Acad Sci USA 78:5744–5748

    Article  CAS  PubMed  Google Scholar 

  • Kuroda-Kawaguchi T, Skaletsky H, Brown LG, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Silber S, Oates R, Rozen S et al (2001) The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat Genet 29:279–286

    Article  CAS  PubMed  Google Scholar 

  • Kuroki Y, Toyoda A, Noguchi H, Taylor TD, Itoh T, Kim DS, Choi SH, Kim IC, Choi HH, Kim YS et al (2006) Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nature Genet 38:158–167

    Article  CAS  PubMed  Google Scholar 

  • Lahn BT, Page DC (1999) Four evolutionary strata on the San Francisco human X chromosome. Science 286:964–967

    Article  CAS  PubMed  Google Scholar 

  • Laursen HB, Jorgensen AL, Jones C, Bak AL (1992) Higher rate of evolution of X chromosome alpha repeat DNA in human than in great apes. EMBO J 11:2367–2372

    CAS  PubMed  Google Scholar 

  • Liu GE, Alkan C, Jiang L, Zhao S, Eichler EE (2009) Comparative analysis of Alu repeats in primate genomes. Genome Res 19:876–885

    Article  CAS  PubMed  Google Scholar 

  • Lohe AE, Brutlag DL (1987) Adjacent satellite DNA segments in Drosophila. Structure of junctions. J Mol Biol 194:171–179

    Article  CAS  PubMed  Google Scholar 

  • Maio JJ (1971) DNA strand reassociation and polyribonucleotide binding in the African green monkey Cercopithecus aethiops. J Mol Biol 56:579–595

    Article  CAS  PubMed  Google Scholar 

  • Manuelidis L, Wu JC (1978) Homology between human and simian repeated DNA. Nature 276:92–94

    Article  CAS  PubMed  Google Scholar 

  • Marshall Graves JA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914

    Article  CAS  Google Scholar 

  • McConkey EA (2002) A project on gene expression during primate development is urgently needed. Trends Genet 18:446

    Article  PubMed  Google Scholar 

  • McConkey EH, Fouts R, Goodman M, Nelson D, Penny D, Ruvolo M, Sikela J, Stewart CB, Varki A, Wise S (2000) Proposal for a human genome evolution project. Mol Phylogenet Evol 15:1–4

    Article  CAS  PubMed  Google Scholar 

  • Mikkelsen TS, Hillier LW, Eichler EE, Zody MC, Jaffe DB, Yang SP, Enard W, Hellmann I, Lindblad-Toth K, Altheide TK et al (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87

    Article  CAS  Google Scholar 

  • Mitchell AR, Gosden JR, Miller DA (1985) A cloned sequence, p82H, of the alphoid repeated DNA family found at the centromeres of all human chromosomes. Chromosoma 92:369–377

    Article  CAS  PubMed  Google Scholar 

  • Muller HJ (1914) A gene for the fourth chromosome of Drosophila. J Exp Zool 17:325–336

    Article  Google Scholar 

  • Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    Article  CAS  PubMed  Google Scholar 

  • Newman TL, Tuzun E, Morrison VA, Hayden KE, Ventura M, McGrath SD, Rocchi M, Eichler EE (2005) A genome-wide survey of structural variation between human and chimpanzee. Genome Res 15:1344–1356

    Article  CAS  PubMed  Google Scholar 

  • Noonan JP, McCallion AS (2010) Genomics of long-range regulatory elements. Annu Rev Genomics Hum Genet 11:1–23

    Article  CAS  PubMed  Google Scholar 

  • Nusbaum C, Mikkelsen TS, Zody MC, Asakawa S, Taudien S, Garber M, Kodira CD, Schueler MG, Shimizu A, Whittaker CA et al (2006) DNA sequence and analysis of human chromosome 8. Nature 439:331–335

    Article  CAS  PubMed  Google Scholar 

  • Oakey R, Tyler-Smith C (1990) Y chromosome haplotyping suggests that most European and Asian men are descended from one or two males. Genomics 7:325–330

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1967) Sex chromosomes and sex linked genes. Springer, New York

    Google Scholar 

  • Olson MV, Varki A (2003) Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet 4:20–28

    Article  CAS  PubMed  Google Scholar 

  • Paar V, Pavin N, Rosandić M, Glunčić M, Basar I, Pezer R, Durajlija Žinić S (2005) ColorHOR—novel graphical algorithm for fast scan of alpha satellite higher-order repeats and HOR annotation for GenBank sequence of human genome. Bioinformatics 21:846–852

    Article  CAS  PubMed  Google Scholar 

  • Paar V, Basar I, Rosandić M, Glunčić M (2007) Consensus higher order repeats and frequency of string distributions in human genome. Curr Genomics 8:93–111

    Article  CAS  PubMed  Google Scholar 

  • Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441:1103–1108

    Article  CAS  PubMed  Google Scholar 

  • Pennacchio LA, Rubin EM (2001) Genomic strategies to identify mammalian regulatory sequences. Nat Rev Genet 2:100–109

    Article  CAS  PubMed  Google Scholar 

  • Perry GH, Tito RY, Verelli BC (2007) The evolutionary history of human and chimpanzee Y-chromosome gene loss. Mol Biol Evol 24:853–859

    Article  CAS  PubMed  Google Scholar 

  • Perry GH, Yang F, Marques-Bonet T, Murphy C, Fitzgerald T, Lee AS, Hyland C, Stone AC, Hurles ME, Tyler-Smith C et al (2008) Copy number variation and evolution in humans and chimpanzees. Genome Res 18:1698–1710

    Article  CAS  PubMed  Google Scholar 

  • Pires-da Silva A, Sommer RJ (2003) The evolution of signalling pathways in animal development. Nat Rev Genet 4:39–49

    Article  CAS  Google Scholar 

  • Pollard KS (2009) What makes us human? Sci Am 300:32–37

    Article  Google Scholar 

  • Pollard KS, Salama SR, King B, Kern AD, Dreszer T, Katzman S, Siepel A, Pedersen JS, Bejerano G, Baertsch R et al (2006a) Forces shaping the fastest evolving regions in the human genome. PLoS Genet 2:1599–1611

    CAS  Google Scholar 

  • Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, Pedersen JS, Katzman S, King B, Onodera C, Siepel A et al (2006b) An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443:167–172

    Article  CAS  PubMed  Google Scholar 

  • Popesco MC, MacLaren EJ, Hopkins J, Dumas L, Cox M, Meltesen L, McGavran L, Wyckoff GJ, Sikela JM (2006) Human lineage-specific amplification, selection, and neuronal expression of DUF1220 domains. Science 313:1304–1307

    Article  CAS  PubMed  Google Scholar 

  • Prabhakar S, Noonan JP, Paabo S, Rubin EM (2006) Accelerated evolution of conserved noncoding sequences in humans. Science 314:786

    Article  CAS  PubMed  Google Scholar 

  • Romanova LY, Deriagin GV, Mashkova TD, Tumeneva IG, Mushegian AR, Kisselev LL, Alexandrov IA (1996) Evidence for selection of alpha satellite DNA: the central role of CENP-B/pJα binding region. J Mol Biol 261:334–340

    Article  CAS  PubMed  Google Scholar 

  • Rosandić M, Paar V, Basar I (2003a) Key-string segmentation algorithm and higher-order repeat 16mer (54 copies) in human alpha satellite DNA in chromosome 7. J Theor Biol 221:29–37

    Article  PubMed  CAS  Google Scholar 

  • Rosandić M, Paar V, Glunčić M, Basar I, Pavin N (2003b) Key-string algorithm - Novel approach to computational analysis of repetitive sequences in human centromeric DNA. Croat Med J 44:386–406

    PubMed  Google Scholar 

  • Rosandić M, Paar V, Basar I, Glunčić M, Pavin N, Pilaš I (2006) CENP-B box and pJα sequence distribution in human alpha satellite higher-order repeats (HOR). Chromosome Res 14:735–753

    Article  PubMed  CAS  Google Scholar 

  • Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H, Marszalek JD, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Page DC (2003) Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423:873–876

    Article  CAS  PubMed  Google Scholar 

  • Rudd MK, Willard HF (2004) Analysis of the centromeric regions of the human genome assembly. Trends Genet 20:529–533

    Article  CAS  PubMed  Google Scholar 

  • Rudd MK, Schueller MG, Willard HF (2003) Sequence organization and functional annotation of human centromeres. Cold Spring Harb Symp Quant Biol 68:141–149

    Article  CAS  PubMed  Google Scholar 

  • Rudd MK, Wray GA, Willard HF (2006) The evolutionary dynamics of alpha-satellite. Genome Res 16:88–96

    Article  CAS  PubMed  Google Scholar 

  • Saxena R, Brown LG, Hawkins T, Alagappan RK, Skaletsky H, Reeve MP, Reijo R, Rozen S, Dinulos MB, Disteche CM, Page DC (1996) The DAZ gene cluster on the human Y chromosome arose from an autosomal gene that was transposed, repeatedly amplified and pruned. Nature Genet 14:292–299

    Article  CAS  PubMed  Google Scholar 

  • Saxena R, De Vries JWA, Repping S, Alagappan RK, Skaletsky H, Brown LG, Ma P, Chen E, Hoovers JMN, Page DC (2000) Four genes in two clusters found in the AZFc region of the human Y chromosome. Genomics 67:256–267

    Article  CAS  PubMed  Google Scholar 

  • Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115

    Article  CAS  PubMed  Google Scholar 

  • Seboun E, Barbaux S, Bourgeron T, Nishi S, Agulnik A, Agasshira M, Nikkawa N, Bishop C, Fellous M, McElreavey K et al (1997) Gene sequence, localization, and evolutionary conservation of DAZL1 A, a candidate male sterility gene. Genomics 41:227–235

    Article  CAS  PubMed  Google Scholar 

  • Sibley CG, Ahlquist JE (1987) DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. J Mol Evol 26:99–121

    Article  CAS  PubMed  Google Scholar 

  • Silber SJ, Repping S (2002) Transmission of male infertility to future generations: lessons from the Y chromosome. Hum Reprod Upd 8:217–229

    Article  Google Scholar 

  • Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837

    Article  CAS  PubMed  Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossing over. Science 191:528–535

    Article  CAS  PubMed  Google Scholar 

  • Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10

    Article  CAS  PubMed  Google Scholar 

  • Spradling AC (1981) The organization and amplification of two chromosomal domains containing Drosophila chorion genes. Cell 27:193–201

    Article  CAS  PubMed  Google Scholar 

  • Tautz D (2000) Evolution of transcriptional regulation. Curr Opin Genet Dev 10:575–579

    Article  CAS  PubMed  Google Scholar 

  • Tyler-Smith C (1985) Structure of repeated sequences in the centromeric region of the human Y chromosome. Development 101:93–100

    Google Scholar 

  • Tyler-Smith C, Brown WRA (1987) Structure of the major block of alphoid satellite DNA on the human Y chromosome. J Mol Biol 195:457–470

    Article  CAS  PubMed  Google Scholar 

  • Uddin M, Wildman DE, Liu G, Xu W, Johnson RM, Hof PR, Kapatos G, Grossman LI, Goodman M (2004) Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc Natl Acad Sci USA 101:2957–2962

    Article  CAS  PubMed  Google Scholar 

  • Varki A, Altheide TK (2005) Comparing human and chimpanzee genomes: searching for needles in a haystack. Genome Res 15:1746–1758

    Article  CAS  PubMed  Google Scholar 

  • Varki A, Geschwind DH, Eichler EE (2008) Explaining human uniqueness: genome interactions with environment, behavior and culture. Nature Genet 9:749–763

    Article  CAS  Google Scholar 

  • Vowles EJ, Amos W (2006) Quantifying ascertainment bias and species-species length differences in human and chimpanzee microsatellites using genome sequences. Mol Biol Evol 23:598–607

    Article  CAS  PubMed  Google Scholar 

  • Warburton PE, Willard HF (1990) Genomic analysis of sequence variation in tandemly repeated DNA. Evidence for localized homogeneous sequence domains within arrays of α-satellite DNA. J Mol Biol 216:3–16

    Article  CAS  PubMed  Google Scholar 

  • Warburton PE, Willard HF (1996) Evolution of centromeric alpha satellite DNA: molecular organization within and between human and primate chromosomes. In: Jackson M, Strachan T, Dover G (eds) Human Genome Evolution. BIOS Scientific, Oxford, pp 121–145

    Google Scholar 

  • Warburton PE, Haaf T, Gosden J, Lawson D, Willard HF (1996) Characterization of a chromosome-specific chimpanzee alpha satellite subset: evolutionary relationship to subsets on human chromosomes. Genomics 33:220–228

    Article  CAS  PubMed  Google Scholar 

  • Warburton PE, Hasson D, Guillem F, Lescale C, Jin X, Abrusan G (2008) Analysis of the largest tandemly repeated DNA families in the human genome. BMC Genomics 9:533

    Article  PubMed  CAS  Google Scholar 

  • Watanabe H, Fujiyama A, Hattori M, Taylor TD, Toyoda A, Kuroki Y, Noguchi H, BenKahla A, Lehrach H, Sudbrak R et al (2004) DNA sequence and comparative analysis of chimpanzee chromosome 22. Nature 429:382–388

    Article  CAS  PubMed  Google Scholar 

  • Waye JS, Willard HF (1987) Nucleotide sequence heterogeneity of alpha satellite repetitive DNA: a survey of alphoid sequences from different human chromosomes. Nucleic Acids Res 15:7549–7569

    Article  CAS  PubMed  Google Scholar 

  • Webster MT, Smith NG, Ellegren H (2003) Compositional evolution of noncoding DNA in the human and chimpanzee genomes. Mol Biol Evol 20:278–286

    Article  CAS  PubMed  Google Scholar 

  • Willard HF (1985) Chromosome-specific organization of human alpha satellite DNA. Am J Hum Genet 37:524–532

    CAS  PubMed  Google Scholar 

  • Willard HF (1991) Evolution of alpha satellite. Curr Opin Genet Dev 1:509–514

    Article  CAS  PubMed  Google Scholar 

  • Willard HF, Waye JS (1987) Hierarchical order in chromosome-specific human alpha satellite DNA. Trends Genet 3:192–198

    Article  CAS  Google Scholar 

  • Wolfe J, Darling SM, Erickson RP, Craig IW, Buckle VJ, Rigby PWJ, Willard HF, Goodfellow PN (1985) Isolation and characterisation of an alphoid centromeric repeat family from the human Y chromosome. J Mol Biol 182:477–485

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

Authors are grateful to Martin Kreitman and Chris Tyler-Smith for very helpful comments and suggestions.

Author information

Authors and Affiliations

  1. Faculty of Science, University of Zagreb, 10000, Zagreb, Croatia

    Vladimir Paar, Matko Glunčić, Ivan Basar & Mislav Cvitković

  2. Department of Internal Medicine, University Hospital Rebro, University of Zagreb, 10000, Zagreb, Croatia

    Marija Rosandić

  3. Faculty of Electrical Engineering and Computing, 10000, Zagreb, Croatia

    Petar Paar

Authors
  1. Vladimir Paar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matko Glunčić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ivan Basar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marija Rosandić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Petar Paar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mislav Cvitković
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vladimir Paar.

Additional information

V. Paar and M. Glunčić contributed equally to this work.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 964 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Paar, V., Glunčić, M., Basar, I. et al. Large Tandem, Higher Order Repeats and Regularly Dispersed Repeat Units Contribute Substantially to Divergence Between Human and Chimpanzee Y Chromosomes. J Mol Evol 72, 34–55 (2011). https://doi.org/10.1007/s00239-010-9401-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-010-9401-8

Keywords

search

Navigation