Chromosoma

, Volume 117, Issue 2, pp 211–217

Dissection of a Y-autosome translocation in Cryptomys hottentotus (Rodentia, Bathyergidae) and implications for the evolution of a meiotic sex chromosome chain

  • J. L. Deuve
  • N. C. Bennett
  • A. Ruiz-Herrera
  • P. D. Waters
  • J. Britton-Davidian
  • T. J. Robinson
Research Article

Abstract

We describe the outcome of a comprehensive cytogenetic survey of the common mole-rat, Cryptomys hottentotus, based on G and C banding, fluorescence in situ hybridisation and the analysis of meiotic chromosomes using immunostaining of proteins involved in the formation of synaptonemal complex (SCP1 and SCP3). We identified the presence of a Y-autosome translocation that is responsible for a fixed diploid number difference between males (2n = 53) and females (2n = 54), a character that likely defines the C. hottentotus lineage. Immunostaining, combined with C banding of spermatocytes, revealed a linearised sex trivalent with X1 at one end and X2 at the other, with evidence of reduced recombination between Y and X2 that seems to be heterochromatin dependant in the C. hottentotus lineage. We suggest that this could depict the likely initial step in the differentiation of a true neo-X, and that this may mimic an early stage in the mammalian meiotic chain formation, an evolutionary process that has been taken to an extreme in a monotreme mammal, the platypus.

Supplementary material

412_2007_140_Fig1_ESM.gif (86 kb)
Supplementary Fig. 1

Double-colour FISH on C. h. natalensis metaphase chromosomes using H. glaber the chromosome painting probes HGL5+6 detected with Cy3 (in pink) and HGL23 detected with FITC (in green). The hybridised chromosomes numbers refer to the C. h. natalensis karyotype presented Fig. 1. (a) The two HGL23 signals (green) corresponds to pair 26 in the female, while in the male (b), the signal corresponds to the X2 (chromosome 26) and the translocated partner which is fused to the Y. We included the inverted DAPI-stained images to facilitate the identification of the chromosomes. The horizontal scale bars correspond to 100 μm (GIF 87 kb)

412_2007_140_Fig1_ESM.tif (889 kb)
High resolutuin (TIF 909 kb)

References

  1. Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151:1569–1579PubMedGoogle Scholar
  2. Ashley T (2002) X-Autosome translocations, meiotic synapsis, chromosome evolution and speciation. Cytogenet Genome Res 96:33–39PubMedCrossRefGoogle Scholar
  3. Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality. Cambridge University Press, CambridgeGoogle Scholar
  4. Brisset S, Izard V, Misrahi M, Aboura A, Madoux S, Ferlicot S, Schoevaert D, Soufir JC, Frydman R, Tachdjian G (2005) Cytogenetic, molecular and testicular tissue studies in an infertile 45,X male carrying an unbalanced (Y;22) translocation: case report. Hum Reprod 20:2168–2172PubMedCrossRefGoogle Scholar
  5. Burgoyne PS (1982) Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet 61:85–90PubMedCrossRefGoogle Scholar
  6. Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033PubMedCrossRefGoogle Scholar
  7. Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B 355:1563–1572CrossRefGoogle Scholar
  8. Deuve JL, Bennett NC, O'Brien PCM, Ferguson-Smith MA, Faulkes CG, Britton-Davidian J, Robinson TJ (2006) Complex evolution of X and Y autosomal translocations in the giant mole-rat, Cryptomys mechowi (Bathyergidae). Chromosome Res 14:681–691PubMedCrossRefGoogle Scholar
  9. Dobigny G, Ozouf-Costaz C, Bonillo C (2004) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113:34–41PubMedCrossRefGoogle Scholar
  10. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107:2749–2760PubMedGoogle Scholar
  11. Faulkes CG, Verheyen E, Verheyen W, Jarvis JUM, Bennett NC (2004) Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae). Mol Ecol 13:613–629PubMedCrossRefGoogle Scholar
  12. Fredga K (1972) Comparative chromosome studies in mongooses (Carnivora, Viverridae). I. Idiograms of 12 species and karyotype evolution in Herpestinae. Hereditas 1:1–74Google Scholar
  13. Gruetzner F, Rens W, Tsend-Ayush E, El-Mogharbel N, O'Brien PCM, Jones RC, Ferguson-Smith MA, Graves JAM (2004) In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432:913–917CrossRefGoogle Scholar
  14. Gruetzner F, Ashley T, Rowell DM, Marshall Graves JA (2006) How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals. Chromosoma 115:75–88PubMedCrossRefGoogle Scholar
  15. Hsu LYF (1994) Phenotype/Karyotype correlations of Y chromosome aneuploidy with emphasis on structural aberrations in postnatally diagnosed cases. Am J Med Genet 53:108–140PubMedCrossRefGoogle Scholar
  16. Iannuzzi L, Molteni L, Di Meo GP, De Giovanni A, Perucatti A, Succi G, Incarnato D, Eggen A, Cribiu EP (2001) A case of azoospermia in a bull carrying a Y-autosome reciprocal translocation. Cytogenet Cell Genet 95:225–227PubMedCrossRefGoogle Scholar
  17. Ingram CM, Burda H, Honeycutt RL (2004) Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys Gray, 1864. Mol Phylogenet Evol 31:997–1014PubMedCrossRefGoogle Scholar
  18. King M (1993) Species evolution: the role of chromosomal change. Cambridge University, CambridgeGoogle Scholar
  19. Lammers JHM, Offenberg HH, van Aalderen M, Vink ACG, Dietrich AJJ, Heyting C (1994) The gene encoding a major component of the lateral element of the synaptonemal complex of the rat is related to X-linked lymphocyte-regulating genes. Mol Cell Biol 14:1137–1146PubMedGoogle Scholar
  20. Matthey R (1964) Un type nouveau de chromosomes sexuels multiples chez une souris Africaine du groupe Mus (Leggada) minutoides (Mammalia-Rodentia). Chromosoma 16:351–364CrossRefGoogle Scholar
  21. Meuwissen TLJ, Offenberg HH, Dietrich AJJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11:5091–5100PubMedGoogle Scholar
  22. Moses MJ (1956) Chromosomal structures in crayfish spermatocytes. J Biophys Biochem Cytol 2:215–218PubMedCrossRefGoogle Scholar
  23. Moses MJ (1969) Structure and function of the synaptonemal complex. Genetics 61(Suppl):41–45PubMedGoogle Scholar
  24. Mudry MD, Rahn IM, Solari AJ (2001) Meiosis and chromosome painting of sex chromosome systems in Ceboidea. Am J Primatol 54:65–78PubMedCrossRefGoogle Scholar
  25. Nevo E, Capanna E, Corti M, Jarvis JUM, Hickman GC (1986) Karyotype differentiation in the endemic subterranean Mole-rats of South Africa (Rodentia, Bathyergidae). Z Saugetierkd 51:36–49Google Scholar
  26. Petit P, Vermeesch JR, Marynen P, de Meurichy W (1994) Comparative cytogenetic study in the subfamily Tragelaphinae. Proceedings of the 11th European colloquium on cytogenetics of domestic animal, Frederiksberg, Denmark, 2–5 June 1994. pp 109–113Google Scholar
  27. Pieczarka JC, Nagamachi CY (1988) Cytogenetic studies of Aotus from eastern Amazonia: Y/autosome rearrangement. Am J Primatol 14:255–263CrossRefGoogle Scholar
  28. Rens W, Grutzner F, O'Brien PCM, Fairclough H, Graves JAM, Ferguson-Smith MA (2004) Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc Natl Acad Sci U S A 101:16257–16261PubMedCrossRefGoogle Scholar
  29. Roig I, Liebe B, Egozcue J, Cabero L, Garcia M, Scherthan H (2004) Female-specific features of recombinational double-stranded DNA repair in relation to synapsis and telomere dynamics in human oocytes. Chromosoma 113:22–33PubMedCrossRefGoogle Scholar
  30. Sbalqueiro IJ, Mattevi MS, Oliveira LF (1984) An X1X1X2X2/X1X2Y mechanism of sex determination in a South American rodent, Deltamys kempi (Rodentia, Cricetidae). Cytogenet Cell Genet 38:50–55PubMedGoogle Scholar
  31. Scherthan H, Cremer T (1994) Methodology of non isotopic in situ hybridization in embedded tissue sections. Methods Mol Genet 5:223–238Google Scholar
  32. Schmekel K, Meuwissen TLJ, Dietrich AJJ, Vink ACG, van Marle J, van Veen H, Heyting C (1996) Organization of SCP1 protein molecules within synaptonemal complexes of rat. Exp Cell Res 226:20–30PubMedCrossRefGoogle Scholar
  33. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972PubMedCrossRefGoogle Scholar
  34. Stack SM (1984) Heterochromatin, the synaptonemal complex and crossing over. J Cell Sci 71:159–176PubMedGoogle Scholar
  35. Sumner AT (1972) A simple method for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–309PubMedCrossRefGoogle Scholar
  36. Veyrunes F, Catalan J, Sicard B, Robinson TJ, Duplantier J-M, Granjon L, Dobigny G, Britton-Davidian J (2004) Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Murinae; Mus). Chromosome Res 12:369–382PubMedCrossRefGoogle Scholar
  37. Waters PD, Ruiz-Herrera A, Dobigny G, Garcia Caldes M, Robinson TJ (2007) Sex chromosomes of basal placental mammals. Chromosoma 116:511–518Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • J. L. Deuve
    • 1
  • N. C. Bennett
    • 2
  • A. Ruiz-Herrera
    • 1
    • 3
  • P. D. Waters
    • 4
  • J. Britton-Davidian
    • 5
  • T. J. Robinson
    • 1
  1. 1.Evolutionary Genomics Group, Department of Botany and ZoologyUniversity of StellenboschMatielandSouth Africa
  2. 2.Mammal Research Institute, Department of Zoology and EntomologyUniversity of PretoriaPretoriaSouth Africa
  3. 3.Dipartimento di Genetica e MicrobiologiaUniversita’ degli Studi di PaviaPaviaItaly
  4. 4.Comparative Genomics Group, Research School of Biological SciencesThe Australian National UniversityCanberraAustralia
  5. 5.Institut des Sciences de l’Evolution (UMR5554), Génétique and EnvironnementUniversité Montpellier IIMontpellierFrance

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