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Mammalian Genome

, Volume 23, Issue 7–8, pp 454–466 | Cite as

A pronounced evolutionary shift of the pseudoautosomal region boundary in house mice

  • Michael A. WhiteEmail author
  • Akihiro Ikeda
  • Bret A. Payseur
Article

Abstract

The pseudoautosomal region (PAR) is essential for the accurate pairing and segregation of the X and Y chromosomes during meiosis. Despite its functional significance, the PAR shows substantial evolutionary divergence in structure and sequence between mammalian species. An instructive example of PAR evolution is the house mouse Mus musculus domesticus (represented by the C57BL/6J strain), which has the smallest PAR among those that have been mapped. In C57BL/6J, the PAR boundary is located just ~700 kb from the distal end of the X chromosome, whereas the boundary is found at a more proximal position in Mus spretus, a species that diverged from house mice 2–4 million years ago. In this study we used a combination of genetic and physical mapping to document a pronounced shift in the PAR boundary in a second house mouse subspecies, Mus musculus castaneus (represented by the CAST/EiJ strain), ~430 kb proximal of the M. m. domesticus boundary. We demonstrate molecular evolutionary consequences of this shift, including a marked lineage-specific increase in sequence divergence within Mid1, a gene that resides entirely within the M. m. castaneus PAR but straddles the boundary in other subspecies. Our results extend observations of structural divergence in the PAR to closely related subspecies, pointing to major evolutionary changes in this functionally important genomic region over a short time period.

Keywords

Bacterial Artificial Chromosome House Mouse Bacterial Artificial Chromosome Library Chromosome Sequence Pseudoautosomal Region 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank Beth Dumont for useful discussions on meiosis and recombination and Francois Bonhomme and Annie Orth for providing the CIM strain. This research was funded by NSF Grant DEB 0918000. MAW was supported by an NLM training grant in Computation and Informatics in Biology and Medicine to the University of Wisconsin (NLM 2T15LM007359).

Supplementary material

335_2012_9403_MOESM1_ESM.doc (119 kb)
Supplementary material 1 (DOC 119 kb)

References

  1. Anunciado RV, Imamura T, Ohno T, Horio F, Namikawa T (2000) Developing a new model for non-insulin dependent diabetes mellitus (NIDDM) by using the Philippine wild mouse, Mus musculus castaneus. Exp Anim 49(1):1–8PubMedCrossRefGoogle Scholar
  2. Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24(2):94–102PubMedCrossRefGoogle Scholar
  3. Boursot P, Din W, Anand R, Darviche D, Dod B, VonDeimling F, Talwar G, Bonhomme F (1996) Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J Evol Biol 9(4):391–415CrossRefGoogle Scholar
  4. Burgoyne PS (1982) Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet 61(2):85–90PubMedCrossRefGoogle Scholar
  5. Burgoyne PS, Mahadevaiah SK, Sutcliffe MJ, Palmer SJ (1992) Fertility in mice requires X-Y pairing and a Y-chromosomal “spermiogenesis” gene mapping to the long arm. Cell 71(3):391–398PubMedCrossRefGoogle Scholar
  6. Bussell JJ, Pearson NM, Kanda R, Filatov DA, Lahn BT (2006) Human polymorphism and human–chimpanzee divergence in pseudoautosomal region correlate with local recombination rate. Gene 368:94–100PubMedCrossRefGoogle Scholar
  7. Charchar FJ, Svartman M, El-Mogharbel N, Ventura M, Kirby P, Matarazzo MR, Ciccodicola A, Rocchi M, D’Esposito M, Graves JAM (2003) Complex events in the evolution of the human pseudoautosomal region 2 (PAR2). Genome Res 13(2):281–286PubMedCrossRefGoogle Scholar
  8. Chen JF, Lu F, Chen SS, Tao SH (2006) Significant positive correlation between the recombination rate and GC content in the human pseudoautosomal region. Genome 49(5):413–419PubMedCrossRefGoogle Scholar
  9. Cooke HJ, Brown WR, Rappold GA (1985) Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature 317(6039):687–692PubMedCrossRefGoogle Scholar
  10. Dal Zotto L, Quaderi NA, Elliott R, Lingerfelter PA, Carrel L, Valsecchi V, Montini E, Yen CH, Chapman V, Kalcheva I et al (1998) The mouse Mid1 gene: implications for the pathogenesis of Opitz syndrome and the evolution of the mammalian pseudoautosomal region. Hum Mol Genet 7(3):489–499PubMedCrossRefGoogle Scholar
  11. Das PJ, Chowdhary BP, Raudsepp T (2009) Characterization of the bovine pseudoautosomal region and comparison with sheep, goat, and other mammalian pseudoautosomal regions. Cytogenet Genome Res 126(1–2):139–147PubMedCrossRefGoogle Scholar
  12. Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Ann Rev Genomics Hum Genet 10:285–311CrossRefGoogle Scholar
  13. Duret L, Mouchiroud D, Gautier C (1995) Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J Mol Evol 40(3):308–317PubMedCrossRefGoogle Scholar
  14. Ellis N, Goodfellow PN (1989) The mammalian pseudoautosomal region. Trends Genet 5(12):406–410PubMedCrossRefGoogle Scholar
  15. Ellis N, Yen P, Neiswanger K, Shapiro LJ, Goodfellow PN (1990) Evolution of the pseudoautosomal boundary in old world monkeys and great apes. Cell 63(5):977–986PubMedCrossRefGoogle Scholar
  16. Filatov DA, Gerrard DT (2003) High mutation rates in human and ape pseudoautosomal genes. Gene 317(1–2):67–77PubMedCrossRefGoogle Scholar
  17. Freije D, Helms C, Watson MS, Donis-Keller H (1992) Identification of a second pseudoautosomal region near the Xq and Yq telomeres. Science 258(5089):1784–1787PubMedCrossRefGoogle Scholar
  18. Gabriel-Robez O, Rumpler Y, Ratomponirina C, Petit C, Levilliers J, Croquette MF, Couturier J (1990) Deletion of the pseudoautosomal region and lack of sex-chromosome pairing at pachytene in two infertile men carrying an X;Y translocation. Cytogenet Cell Genet 54(1–2):38–42PubMedCrossRefGoogle Scholar
  19. Galtier N (2004) Recombination, GC-content and the human pseudoautosomal boundary paradox. Trends Genet 20(8):347–349PubMedCrossRefGoogle Scholar
  20. Gaudenz K, Roessler E, Quaderi N, Franco B, Feldman G, Gasser DL, Wittwer B, Horst J, Montini E, Opitz JM et al (1998) Opitz G/BBB syndrome in Xp22: mutations in the MID1 gene cluster in the carboxy-terminal domain. Am J Hum Genet 63(3):703–710PubMedCrossRefGoogle Scholar
  21. Geraldes A, Basset P, Gibson B, Smith KL, Harr B, Yu H-T, Bulatova N, Ziv Y, Nachman MW (2008) Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol 17(24):5349–5363PubMedCrossRefGoogle Scholar
  22. Graves JA (1995) The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci 350(1333):305–311PubMedCrossRefGoogle Scholar
  23. Graves JA, Wakefield MJ, Toder R (1998) The origin and evolution of the pseudoautosomal regions of human sex chromosomes. Hum Mol Genet 7(13):1991–1996PubMedCrossRefGoogle Scholar
  24. Guénet JL, Nagamine C, Simon-Chazottes D, Montagutelli X, Bonhomme F (1990) Hst-3: an X-linked hybrid sterility gene. Genet Res 56(2–3):163–165PubMedCrossRefGoogle Scholar
  25. Hale DW, Washburn LL, Eicher E (1993) Meiotic abnormalities in hybrid mice of the C57BL/6J × Mus spretus cross suggest a cytogenetic basis for Haldane’s rule of hybrid sterility. Cytogenet Cell Genet 63(4):221–234PubMedCrossRefGoogle Scholar
  26. Harbers K, Soriano P, Müller U, Jaenisch R (1986) High frequency of unequal recombination in pseudoautosomal region shown by proviral insertion in transgenic mouse. Nature 324(6098):682–685PubMedCrossRefGoogle Scholar
  27. Hasegawa M, Kishino H, Yano T (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174PubMedCrossRefGoogle Scholar
  28. Hobolth A, Christensen OF, Mailund T, Schierup MH (2007) Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3(2):e7PubMedCrossRefGoogle Scholar
  29. Huang SW, Friedman R, Yu N, Yu A, Li WH (2005) How strong is the mutagenicity of recombination in mammals? Mol Biol Evol 22(3):426–431PubMedCrossRefGoogle Scholar
  30. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755PubMedCrossRefGoogle Scholar
  31. Ishikawa A, Matsuda Y, Namikawa T (2000) Detection of quantitative trait loci for body weight at 10 weeks from Philippine wild mice. Mamm Genome 11(10):824–830PubMedCrossRefGoogle Scholar
  32. Iwase M, Satta Y, Hirai Y, Hirai H, Imai H, Takahata N (2003) The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species. Proc Natl Acad Sci USA 100(9):5258–5263PubMedCrossRefGoogle Scholar
  33. Iwase M, Kaneko S, Kim H, Satta Y, Takahata N (2007) Evolutionary history of sex-linked mammalian amelogenin genes. Cells Tissues Organs 186(1):49–59PubMedCrossRefGoogle Scholar
  34. Janaswami PM, Birkenmeier EH, Cook SA, Rowe LB, Bronson RT, Davisson MT (1997) Identification and genetic mapping of a new polycystic kidney disease on mouse chromosome 8. Genomics 40(1):101–107PubMedCrossRefGoogle Scholar
  35. Kasahara T, Abe K, Mekada K, Yoshiki A, Kato T (2010) Genetic variation of melatonin productivity in laboratory mice under domestication. Proc Natl Acad Sci USA 107(14):6412–6417PubMedCrossRefGoogle Scholar
  36. Keane TM, Goodstadt L, Danecek P, White MA, Wong K, Yalcin B, Heger A, Agam A, Slater G, Goodson M et al (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477(7364):289–294PubMedCrossRefGoogle Scholar
  37. Keitges E, Rivest M, Siniscalco M, Gartler SM (1985) X-linkage of steroid sulphatase in the mouse is evidence for a functional Y-linked allele. Nature 315(6016):226–227PubMedCrossRefGoogle Scholar
  38. Kent WJ (2002) BLAT: the BLAST-like alignment tool. Genome Res 12(4):656–664PubMedGoogle Scholar
  39. Kipling D, Salido EC, Shapiro LJ, Cooke HJ (1996a) High frequency de novo alterations in the long-range genomic structure of the mouse pseudoautosomal region. Nat Genet 13(1):78–80PubMedCrossRefGoogle Scholar
  40. Kipling D, Wilson HE, Thomson EJ, Lee M, Perry J, Palmer S, Ashworth A, Cooke HJ (1996b) Structural variation of the pseudoautosomal region between and within inbred mouse strains. Proc Natl Acad Sci USA 93(1):171–175PubMedCrossRefGoogle Scholar
  41. Kvaløy K, Galvagni F, Brown WR (1994) The sequence organization of the long arm pseudoautosomal region of the human sex chromosomes. Hum Mol Genet 3(5):771–778PubMedCrossRefGoogle Scholar
  42. Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286(5441):964–967PubMedCrossRefGoogle Scholar
  43. Lancioni A, Pizzo M, Fontanella B, Ferrentino R, Napolitano LMR, De Leonibus E, Meroni G (2010) Lack of Mid1, the mouse ortholog of the Opitz syndrome gene, causes abnormal development of the anterior cerebellar vermis. J Neurosci 30(8):2880–2887PubMedCrossRefGoogle Scholar
  44. Lyons MA, Wittenburg H, Li R, Walsh KA, Leonard MR, Korstanje R, Churchill GA, Carey MC, Paigen B (2003) Lith6: a new QTL for cholesterol gallstones from an intercross of CAST/Ei and DBA/2J inbred mouse strains. J Lipid Res 44(9):1763–1771PubMedCrossRefGoogle Scholar
  45. Lyons MA, Wittenburg H, Li R, Walsh KA, Korstanje R, Churchill GA, Carey MC, Paigen B (2004) Quantitative trait loci that determine lipoprotein cholesterol levels in an intercross of 129S1/SvImJ and CAST/Ei inbred mice. Physiol Genomics 17(1):60–68PubMedCrossRefGoogle Scholar
  46. Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19(6):330–338PubMedCrossRefGoogle Scholar
  47. Matsuda Y, Imai HT, Moriwaki K, Kondo K, Bonhomme F (1982) X-Y chromosome dissociation in wild derived Mus musculus subspecies, laboratory mice, and their F1 hybrids. Cytogenet Cell Genet 34(3):241–252PubMedCrossRefGoogle Scholar
  48. Matsuda Y, Hirobe T, Chapman VM (1991) Genetic basis of X-Y chromosome dissociation and male sterility in interspecific hybrids. Proc Natl Acad Sci USA 88(11):4850–4854PubMedCrossRefGoogle Scholar
  49. Matsuda Y, Moens PB, Chapman VM (1992) Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma 101(8):483–492PubMedCrossRefGoogle Scholar
  50. Mohandas TK, Speed RM, Passage MB, Yen PH, Chandley AC, Shapiro LJ (1992) Role of the pseudoautosomal region in sex-chromosome pairing during male meiosis: meiotic studies in a man with a deletion of distal Xp. Am J Hum Genet 51(3):526–533PubMedGoogle Scholar
  51. Montoya-Burgos JI, Boursot P, Galtier N (2003) Recombination explains isochores in mammalian genomes. Trends Genet 19(3):128–130PubMedCrossRefGoogle Scholar
  52. Palmer S, Perry J, Ashworth A (1995) A contravention of Ohno’s law in mice. Nat Genet 10(4):472–476PubMedCrossRefGoogle Scholar
  53. Palmer S, Perry J, Kipling D, Ashworth A (1997) A gene spans the pseudoautosomal boundary in mice. Proc Natl Acad Sci USA 94(22):12030–12035PubMedCrossRefGoogle Scholar
  54. Pamilo P, Bianchi NO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10(2):271–281PubMedGoogle Scholar
  55. Perry J, Ashworth A (1999) Evolutionary rate of a gene affected by chromosomal position. Curr Biol 9(17):987–989PubMedCrossRefGoogle Scholar
  56. Perry J, Palmer S, Gabriel A, Ashworth A (2001) A short pseudoautosomal region in laboratory mice. Genome Res 11(11):1826–1832PubMedGoogle Scholar
  57. Posada D, Buckley T (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53(5):793–808PubMedCrossRefGoogle Scholar
  58. Quaderi NA, Schweiger S, Gaudenz K, Franco B, Rugarli EI, Berger W, Feldman GJ, Volta M, Andolfi G, Gilgenkrantz S et al (1997) Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat Genet 17(3):285–291PubMedCrossRefGoogle Scholar
  59. Rattray AJ, McGill CB, Shafer BK, Strathern JN (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158(1):109–122PubMedGoogle Scholar
  60. Raudsepp T, Chowdhary BP (2008) The horse pseudoautosomal region (PAR): characterization and comparison with the human, chimp and mouse PARs. Cytogenet Genome Res 121(2):102–109PubMedCrossRefGoogle Scholar
  61. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574PubMedCrossRefGoogle Scholar
  62. 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(7031):325–337PubMedCrossRefGoogle Scholar
  63. Rouyer F, Simmler MC, Johnsson C, Vergnaud G, Cooke HJ, Weissenbach J (1986) A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319(6051):291–295PubMedCrossRefGoogle Scholar
  64. Rugarli EI, Adler DA, Borsani G, Tsuchiya K, Franco B, Hauge X, Disteche C, Chapman V, Ballabio A (1995) Different chromosomal localization of the Clcn4 gene in Mus spretus and C57BL/6J mice. Nat Genet 10(4):466–471PubMedCrossRefGoogle Scholar
  65. Salcedo T, Geraldes A, Nachman MW (2007) Nucleotide variation in wild and inbred mice. Genetics 177(4):2277–2291PubMedCrossRefGoogle Scholar
  66. Salido EC, Li XM, Yen PH, Martin N, Mohandas TK, Shapiro LJ (1996) Cloning and expression of the mouse pseudoautosomal steroid sulphatase gene (Sts). Nat Genet 13(1):83–86PubMedCrossRefGoogle Scholar
  67. Schiebel K, Meder J, Rump A, Rosenthal A, Winkelmann M, Fischer C, Bonk T, Humeny A, Rappold G (2000) Elevated DNA sequence diversity in the genomic region of the phosphatase PPP2R3L gene in the human pseudoautosomal region. Cytogenet Cell Genet 91(1–4):224–230PubMedCrossRefGoogle Scholar
  68. She JX, Bonhomme F, Boursot P, Thaler L, Catzeflis F (1990) Molecular phylogenies in the genus Mus: comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP data. Biol J Linn Soc 41(1–3):83–103CrossRefGoogle Scholar
  69. Shi Q, Spriggs E, Field LL, Ko E, Barclay L, Martin RH (2001) Single sperm typing demonstrates that reduced recombination is associated with the production of aneuploid 24, XY human sperm. Am J Med Genet 99(1):34–38PubMedCrossRefGoogle Scholar
  70. Simmler MC, Rouyer F, Vergnaud G, Nyström-Lahti M, Ngo KY, de la Chapelle A, Weissenbach J (1985) Pseudoautosomal DNA sequences in the pairing region of the human sex chromosomes. Nature 317(6039):692–697PubMedCrossRefGoogle Scholar
  71. 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(6942):825–837PubMedCrossRefGoogle Scholar
  72. Soriano P, Keitges EA, Schorderet DF, Harbers K, Gartler SM, Jaenisch R (1987) High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci USA 84(20):7218–7220PubMedCrossRefGoogle Scholar
  73. Strathern JN, Shafer BK, McGill CB (1995) DNA synthesis errors associated with double-strand-break repair. Genetics 140(3):965–972PubMedGoogle Scholar
  74. Suzuki H, Shimada T, Terashima M, Tsuchiya K, Aplin K (2004) Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 33(3):626–646PubMedCrossRefGoogle Scholar
  75. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  76. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599PubMedCrossRefGoogle Scholar
  77. Van Laere AS, Coppieters W, Georges M (2008) Characterization of the bovine pseudoautosomal boundary: Documenting the evolutionary history of mammalian sex chromosomes. Genome Res 18(12):1884–1895PubMedCrossRefGoogle Scholar
  78. White MA, Ané C, Dewey CN, Larget BR, Payseur BA (2009) Fine-scale phylogenetic discordance across the house mouse genome. PLoS Genet 5(11):e1000729PubMedCrossRefGoogle Scholar
  79. White MA, Stubbings M, Dumont BL, Payseur BA (2012) Genetics and evolution of hybrid male sterility in house mice. Genetics 191(3)Google Scholar
  80. Winter J, Lehmann T, Krauss S, Trockenbacher A, Kijas Z, Foerster J, Suckow V, Yaspo M-L, Kulozik A, Kalscheuer V et al (2004) Regulation of the MID1 protein function is fine-tuned by a complex pattern of alternative splicing. Hum Genet 114(6):541–552PubMedCrossRefGoogle Scholar
  81. Yi S, Summers TJ, Pearson NM, Li WH (2004) Recombination has little effect on the rate of sequence divergence in pseudoautosomal boundary 1 among humans and great apes. Genome Res 14(1):37–43PubMedCrossRefGoogle Scholar
  82. Yi N, Zinniel DK, Kim K, Eisen EJ, Bartolucci A, Allison DB, Pomp D (2006) Bayesian analyses of multiple epistatic QTL models for body weight and body composition in mice. Genet Res 87(1):45–60PubMedCrossRefGoogle Scholar
  83. Young AC, Kirkness EF, Breen M (2008) Tackling the characterization of canine chromosomal breakpoints with an integrated in-situ/in-silico approach: the canine PAR and PAB. Chromosome Res 16(8):1193–1202PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Michael A. White
    • 1
    • 2
    Email author
  • Akihiro Ikeda
    • 1
  • Bret A. Payseur
    • 1
  1. 1.Laboratory of GeneticsUniversity of WisconsinMadisonUSA
  2. 2.Division of Human BiologyFred Hutchinson Cancer Research CenterSeattleUSA

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