Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Anatomy and chromosomes of two intersexual dasyurid marsupials

P. A. Woolley A D , N. Guedelha B E and J. A. M. Graves B C
+ Author Affiliations
- Author Affiliations

A Department of Zoology, La Trobe University Bundoora, Vic. 3086, Australia.

B Department of Genetics, La Trobe University Bundoora, Vic. 3086, Australia.

C Present address: Research School of Biological Sciences, The Australian National University, Canberra, ACT 2601, Australia.

D To whom correspondence should be addressed. email: p.woolley@latrobe.edu.au

E *N. Guedelha’s contribution to this paper was the investigation of the Sminthopsis douglasi karyotypes.

Reproduction, Fertility and Development 15(5) 293-301 https://doi.org/10.1071/RD03045
Submitted: 4 July 2003  Accepted: 2 September 2003   Published: 2 September 2003

Abstract

The intersexual phenotypes of marsupials with XXY and XO chromosome constitutions imply that not all sexual dimorphisms are under the control of testicular hormones and, ultimately, the SRY gene on the Y chromosome. It has been hypothesised that there is a gene on the X chromosome that determines whether either a scrotum will form (one copy of the gene) or a pouch with teats (two copies of the gene). Here, we describe the anatomy and chromosomes of two intersexual dasyurid marsupials. One, a Dasyuroides byrnei, had a pouch, but the reproductive tract was essentially male. The other, a Sminthopsis douglasi, had a hemipouch and a hemiscrotum and the reproductive tract was essentially female. The S. douglasi was a mosaic for cells with an apparently normal 2n = 14, XX female karyotype and cells with 2n = 14 plus (usually) two dot-like supernumerary elements 2n = 14, XX + 2B. The D. byrnei cells examined also had a 2n = 14, XX + 2B karyotype. In fibroblasts from the male and female sides of the S. douglasi, it was possible to assign the 2n = 14, XX karyotype to the male side and the 2n = 14, XX + 2B to the female side.

Extra keywords: chromosome abnormalities, pouch/scrotum differentiation.


Acknowledgments

This work was performed with financial support from La Trobe University, the Living Together Foundation (to P.A.W.) and the Australian Research Council (to J.A.M.G.) and with La Trobe University Animal Ethics Committee approval (no. LSB96/4/V3). We thank Harold Attwood for provision of photographs of the chromosomes of the intersexual D. byrnei, Michael Westerman for the photograph of the chromosomes of the normal male D. byrnei, Iole Barbieri for S. douglasi cell culture, Frank Gruetzner for help with imaging of S. douglasi chromosomes, Alan Wright for photomicrography and Trevor Phillips for preparation of the illustrations.


References

Cooper, D. W. (1993). The evolution of sex determination, sex chromosome dimorphism and X-inactivation in therian mammals: a comparison of metatherians (marsupials) and eutherians (‘placentals’). In ‘Sex Chromosomes and Sex Determining Genes’. (Eds. K. C. Reed and J. A. M. Graves)  pp. 183–98. (Harwood Academic Publishers: Chur, Switzerland.)

Cooper, D. W. , Johnston, P. G. , Graves, J. A. M. , and Watson, J. M. (1993). X-inactivation in marsupials and monotremes. Semin. Dev. Biol. 4, 117–28.
Crossref | GoogleScholarGoogle Scholar |

Ford, C. E. , Jones, K. W. , Polani, P. E. , de Almeida, J. C. , and Briggs, J. H. (1959). A sex chromosome anomaly in the case of gonadal dysgenesis. Lancet i, 711–13.
Crossref | GoogleScholarGoogle Scholar |

Foster, J. W. , Brennan, F. E. , Hampikian, G. K. , Goodfellow, P. N. , Sinclair, A. H. , Lovell-Badge, R. , Selwood, L. , Renfree, M. B. , Cooper, D. W. , and Graves, J. A. M. (1992). Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature 359, 531–33.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Graves, J. A. M. (1967). DNA synthesis in chromosomes of cultured leucocytes from two marsupial species. Exp. Cell Res. 46, 37–47.
PubMed |

Hughes, R. L., Pearse, A. M., Cooper, D. W., Joss, J. M. P., Johnston, P. G. and  Jones, M. K. (1993). The genetic basis of marsupial gonadogenesis and sexual phenotype. In ‘Sex Chromosomes and Sex Determining Genes’. (Eds. K. C. Reed and J. A. M. Graves.)  pp. 7–48. (Harwood Academic Publishers: Chur, Switzerland.)

Jacobs, P. A. , and Strong, J. A. (1959). A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183, 302–3.
PubMed |

O, W.-S. , Renfree, M. B. , Short, R. V. , and Shaw, G. (1988). Primary genetic control of somatic sexual differentiation in a mammal. Nature 331, 716–17.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Renfree, M. B. , and Short, R. V. (1988). Sex determination in marsupials: evidence for a marsupial–eutherian dichotomy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 322, 41–53.
PubMed |

Santucciu, G. , Grutzner, F. , Carvalho, D. R. , and Graves, J. A. M. (). Isolation of chromosomal regions controlling intersex development in a marsupial. Cytogenet. Genome Res. ,(in press)
Crossref | GoogleScholarGoogle Scholar |

Sharman, G. B. , Robinson, E. S. , Walton, E. S. , and Berger, P. J. (1970). Sex chromosomes and reproductive anatomy of some intersexual marsupials. J. Reprod. Fertil. 21, 57–68.
PubMed |

Sharman, G. B. , Hughes, R. L. , and Cooper, D. W. (1990). The chromosomal basis of sex differentiation in marsupials. Aust. J. Zool. 37, 451–66.


Sinclair, A. H. , Berta, P. , Palmer, M. S. , Hawkins, J. R. , Griffiths, B. L. , Smith, M. J. , Foster, J. W. , Frischauf, A.-M. , Lovell-Badge, R. , and Goodfellow, P. N. (1990). A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240–4.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Watson, C. M. , Johnston, P. G. , Rodger, K. A. , McKenzie, L. M. , O’Neill, R. J. , and Cooper, D. W. (1997). SRY and karyotypic status of one abnormal and two intersexual marsupials. Reprod. Fertil. Dev. 9, 233–41.
PubMed |

Westerman, M. , and Woolley, P. A. (1990). Cytogenetics of some New Guinean dasyurids and genome evolution in the Dasyuridae (Marsupialia). Aust. J. Zool. 37, 521–31.


Westerman, M. , and Woolley, P. A. (1993). Chromosomes and the evolution of dasyurid marsupials: an overview. Sci. New Guinea 19, 123–30.


Woolley, P. A. (1971). Maintenance and breeding of laboratory colonies of Dasyuroides byrnei and Dasycercus cristicauda.  Int. Zoo Yearbook 11(54), 351–4.


Young, G. J., Graves, J. A. M., Barbieri, I., Woolley, P. A., Cooper, D. W. and  Westerman, M. (1982). The chromosomes of dasyurids (Marsupialia). In ‘Carnivorous Marsupials’. (Ed M. Archer)  pp. 783–95. (Royal Zoological Society of New South Wales: Sydney.)