Chromosome Research

, Volume 7, Issue 6, pp 461–474 | Cite as

Karyotype Relationships Between Four Distantly Related Marsupials Revealed by Reciprocal Chromosome Painting

  • W. Rens
  • P. C. M. O'Brien
  • F. Yang
  • J. A. M. Graves
  • M. A. Ferguson-Smith

Abstract

Marsupial karyotypes have shown extensive conservation even between distantly related groups with a high diversity of life forms and reproductive biology. Banding analysis has been the main test for assessing their homologies and chromosome rearrangements. More recently, cross-species reciprocal chromosome painting has been developed and applied to several mammalian species and has shown homologies and rearrangements not revealed by banding analysis. Karyotype relationships between four marsupial species, Sminthopsis crassicaudata, Potorous tridactylus, Trichosurus vulpecula and Macropus eugenii, which are from different families in two orders, were investigated and presented in the form of comparative chromosome maps. These show that only a limited number of chromosomal rearrangements have occurred during their evolution. A karyotype phylogeny of the four marsupials was derived from these maps. A comparison between published gene location and the comparative chromosome maps for these species is presented and inconsistencies with previous gene mapping data indicated.

chromosomal homology chromosome painting Macropus eugenii marsupials Potorous tridactylus Sminthopsis crassicaudata Trichosurus vulpecula 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arnold N, Stanyon R, Jauch A, O'Brien PCM, Wienberg J (1996) Identification of complex chromosome rearrangements in the gibbon by fluorescence in situ hybridization (FISH) of a human chromosome 2q specific microlibrary, yeast artificial chromosomes, and reciprocal chromosome painting. Cytogenet Cell Genet 74: 80–85.Google Scholar
  2. Burke A, Westerman M, Springer M (1998) The phylogenetic position of Hypsiprymnodon moschatus and the evolution of bipedal hopping in kangaroos (Macropodidae: Diprodontia). System Biol 47: 457–474.Google Scholar
  3. Burkin DJ, O'Brien PCM, Broad TE et al. (1997) Isolation of chromosome-specific paints from high resolution flow karyotypes of the sheep (Ovis aries). Chromosome Res 5: 102–108.Google Scholar
  4. Eldridge MDB, Close RL (1993) Radiation of chromosome shuffles. Curr Opin Genet Dev 3: 915–922.Google Scholar
  5. Eldridge MDB, Johnston PG, Close RL (1992) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupiala, Macropodidae). Cytogenet Cell Genet 61: 29–33.Google Scholar
  6. Ferguson-Smith MA (1997) Genetic analysis by chromosome sorting and painting: phylogenetic and diagnostic applications. Eur J Hum Genet 5: 253–265.Google Scholar
  7. Fitzgerald J, Wilcox SA, Graves JAM, Dahl HHM (1993) A eutherian X-linked gene, PDHA1, is autosomal in marsupials: a model for the evolution of a second, testis-specific variant in eutherian mammals. Genomics 18: 636–642.Google Scholar
  8. Glas R, De Leo A, Reid K, Ferguson-Smith MA et al. (1999) Chromosome painting in the kangaroo family: Macropodidae. Chromosome Res 7: 167–176.Google Scholar
  9. Goureau A, Yerle M, Schmitz A et al. (1996) Human and porcine correspondence of chromosome segments using bidirectional chromosome painting. Genomics 36: 252–262.Google Scholar
  10. Hayman DL, Martin PG (1974) Marsupial Cytogenetics. Berlin: Gebruder Borntraeger.Google Scholar
  11. Jauch A, Wienberg J, Stanyon R et al. (1992) Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proc Natl Acad Sci USA 89: 8611–8615.Google Scholar
  12. Kirsch JAW, Lapointe FJ, Springer MS (1996) DNA-hybridization studies of marsupials and their implications for metatherian classification. Aust J Zool 45: 211–280.Google Scholar
  13. Koehler U, Bigoni F, Wienberg J, Stanyon R (1995) Genomic reorganization in the concolor gibbon (Hylobates concolor) revealed by chromosome painting. Genomics 30: 287–292.Google Scholar
  14. Langford CF, Telenius H, Miller NG, Thomsen PD, Tucker DM (1993) Preparation of chromosome specific paints and complete assignment of chromosomes in the pig flow karyotype. Anim Genet 24: 261–267.Google Scholar
  15. Langford CF, Fischer PE, Binns MM, Holmes NG, Carter NP (1996) Chromosome specific paints from a high resolution flow karyotype of the dog. Chromosome Res 4: 115–123.Google Scholar
  16. Maccarone P, Watson JM, Francis D, Selwood L, Kola I, Graves JAM (1992) The evolution of human chromosome 21: evidence from in situ hybridization in marsupials and a monotreme. Genomics 13: 1119–1124.Google Scholar
  17. McKay LM, Watson JM, Graves JAM (1992) Mapping human Xlinked genes in the Phalangerid marsupial Trichosurus vulpecula. Genomics 14: 302–308.Google Scholar
  18. Müller S, O'Brien PCM, Ferguson-Smith MA, Wienberg J (1997) Reciprocal chromosome painting between human and prosimian (Eulemar macaco macaco and E. fulvus mayottensis). Cytogenet Cell Genet 78: 260–271.Google Scholar
  19. O'Brien SJ, Wienberg J, Lyons LA (1997) Comparative genomics: lessons from cats. Trends Genet 13,10: 393–399.Google Scholar
  20. O'Neill RJW, Eldridge MDB, Ferguson-Smith MA, O'Brien PC, Graves JAM (1999) Chromosome evolution in kangaroos (Marsupialia: Macropodidae). Cross species chromosome painting between the tammar wallaby and rock wallaby spp. with the 2n = 22 ancestral macropodid karyotype. Genome 14,3: 525–530.Google Scholar
  21. Rabbits P, Impey H, Heppel-Parton A et al. (1995) Chromosome specific paints from a high resolution flow karyotype of the mouse. Natl Genet 9: 369–375.Google Scholar
  22. Rofe RH (1978) G-banded chromosomes and the evolution of Macropodidae. Aust Mammal 2: 53–63.Google Scholar
  23. Rofe RH (1979) G-banding and Chromosomal Evolution in Australian Marsupials. PhD thesis, University of Adelaide, South Australia.Google Scholar
  24. Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in the Marsupiala. Cytogenet Cell Genet 39: 40–50.Google Scholar
  25. Samollow P, Graves JAM (1998) Gene mapping in marsupials. Inst Lab Animal Res J 39: 159–178.Google Scholar
  26. Scherthan H, Cremer T, Arnason U, Weier HU, Lima-de-Faria A, Frönicke L (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Natl Genet 6: 342–347.Google Scholar
  27. Sharman GB (1961) The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust J Zool 9: 38–60.Google Scholar
  28. Sinclair AH, Graves JAM (1991) Gene mapping in marsupials: detection of an ancient autosomal gene cluster. Genomics 9: 581–586.Google Scholar
  29. Spencer JA, Sinclair AH, Watson JM, Graves JAM (1991) Genes on the short arm of the human X chromosome are not shared with the marsupial X. Genomics 11: 339–345.Google Scholar
  30. Stanyon R, Arnold N, Koehler U, Bigoni F, Wienberg J (1995) Chromosomal painting shows that ‘marked chromosomes’ in lesser apes and Old World monkeys are not homologous and evolved by convergence. Cytogenet Cell Genet 68: 74–78.Google Scholar
  31. Svartman M, Vianna-Morgante AM (1998) Karyotype evolution of marsupials: from higher to lower diploid numbers. Cytogenet Cell Genet 82: 263–266.Google Scholar
  32. Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosome Cancer 4: 257–263.Google Scholar
  33. Toder R, Wienberg J, Voullaire L, O'Brien PCM, Maccarone P, Graves JAM (1996) Shared DNA sequences between the X and Y chromosomes in the tammar wallaby — evidence for independent additions to eutherian and marsupial sex chromosomes. Chromosoma 106: 94–98.Google Scholar
  34. Toder R, O'Neill RJW, Wienberg J, O'Brien PCM, Voullaire L, Graves JAM (1997) Comparative chromosome painting between two marsupials: origins of an XX/XY1Y2 sex chromosome system. Mammalian Genome 8: 418–422.Google Scholar
  35. Walen KH, Brown SW (1962) Chromosomes in a marsupial (Potorous tridactylis) tissue culture. Nature 184: 406.Google Scholar
  36. Wienberg J, Jauch A, Stanyon R, Cremer T (1990) Molecular cytotaxonamy of primates by chromosomal in situ suppresion hybridization. Genomics 8: 347–350.Google Scholar
  37. Wienberg J, Stanyon R (1995) Chromosome painting in mammals as an approach to comparative genomics. Curr Opin Genet Dev 5: 792–797.Google Scholar
  38. Wienberg J, Stanyon R (1997) Comparative painting of mammalian chromosomes. Curr Opin Genet Dev 7: 784–791.Google Scholar
  39. Wienberg J, Stanyon R, Nash WG et al. (1997) Conservation of human vs. feline genome organization revealed by reciprocal chromosome painting. Cytogenet Cell Genet 77: 211–217.Google Scholar
  40. Yang F, Carter NP, Shi L, Ferguson-Smith (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642–652.Google Scholar
  41. Yang F, O'Brien PCM, Wienberg J, Neitzel H, Lin CC, Ferguson-Smith MA (1997a) Chromosomal evolution of the Chinese muntjac (Muntiacus reevesi). Chromosoma 106: 37–43.Google Scholar
  42. Yang F, Müller S, Just R, Ferguson-Smith MA, Wienberg J (1997b) Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39: 396–401.Google Scholar
  43. Yang F, O'Brien PCM, Wienberg J, Ferguson-Smith MA (1997c) A reappraisal of the tandem fusion theory of karyotype evolution in the Indian Muntjac using chromosome painting. Chromosome Res 50: 109–117.Google Scholar
  44. Young GJ, Graves JAM, Barbieri I, Woolley PA, Cooper DW, Westerman M (1982) The chromosomes of dasyurids (Marsupialia). In: Archer M, ed. Carnivorous Marsupials, Vol. 2. Royal Zoological Society, NSW, pp 783–795.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • W. Rens
    • 1
  • P. C. M. O'Brien
    • 1
  • F. Yang
    • 1
  • J. A. M. Graves
    • 2
  • M. A. Ferguson-Smith
    • 1
  1. 1.Centre for Veterinary ScienceCambridge UniversityCambridgeUK
  2. 2.School of Biochemistry and GeneticsLa Trobe UniversityMelbourneAustralia

Personalised recommendations