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In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes

Nature volume 432, pages 913–917 (2004)Cite this article

Abstract

Two centuries after the duck-billed platypus was discovered, monotreme chromosome systems remain deeply puzzling. Karyotypes of males1, or of both sexes2,3,4, were claimed to contain several unpaired chromosomes (including the X chromosome) that form a multi-chromosomal chain at meiosis. Such meiotic chains exist in plants5 and insects6 but are rare in vertebrates7. How the platypus chromosome system works to determine sex and produce balanced gametes has been controversial for decades1,2,3,4. Here we demonstrate that platypus have five male-specific chromosomes (Y chromosomes) and five chromosomes present in one copy in males and two copies in females (X chromosomes). These ten chromosomes form a multivalent chain at male meiosis, adopting an alternating pattern to segregate into XXXXX-bearing and YYYYY-bearing sperm. Which, if any, of these sex chromosomes bears one or more sex-determining genes remains unknown. The largest X chromosome, with homology to the human X chromosome, lies at one end of the chain, and a chromosome with homology to the bird Z chromosome lies near the other end. This suggests an evolutionary link between mammal and bird sex chromosome systems, which were previously thought to have evolved independently.

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Figure 1: Fluorescence in situ hybridization (FISH) of chromosome paints on mitotic chromosomes.
Figure 2: Order of chromosomes in the meiotic chain.
Figure 3: The elements of the chain.
Figure 4: Alternate segregation of the chain.

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Acknowledgements

We thank P. Miethke and D. McMillan for technical assistance, D. Zarkower for providing the chicken DMRT1 cDNA and A. Pask for information on SOX genes and SRY in monotremes, and provision of Supplementary Fig. 1. This work was supported by the Australian Research Council (F.G. and J.A.M.G.). W.R. and M.A.F.-S. are supported by a Wellcome Trust grant to the Cambridge Resource Centre for Comparative Genomics. Facilities were provided by Macquarie Generation and Glenrock Station, NSW. Approval to collect animals was granted by the New South Wales National Parks and Wildlife Services, New South Wales Fisheries, Environment Australian Capital Territory and the Animal Experimentation Ethics Committee, Australian National University.

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Author notes

  1. Enkhjargal Tsend-Ayush and Nisrine El-Mogharbel: These authors contributed equally to this work

Authors and Affiliations

  1. Research School of Biological Sciences, Australian National University, Canberra, GPO Box 475, Australian Capital Territory, 2601, Australia

    Frank Grützner, Enkhjargal Tsend-Ayush, Nisrine El-Mogharbel & Jennifer A. Marshall Graves

  2. Centre for Veterinary Science, Department of Veterinary Medicine, University of Cambridge, Madingley Road, CB3 0ES, Cambridge, UK

    Willem Rens, Patricia C. M. O'Brien & Malcolm A. Ferguson-Smith

  3. Department of Biological Sciences, The University of Newcastle, Callaghan, New South Wales, 2308, Australia

    Russell C. Jones

Authors
  1. Frank Grützner
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Corresponding author

Correspondence to Frank Grützner.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Note

Search for Platypus SRY (DOC 31 kb)

Supplementary Figure 1

Male and female platypus DNA cut with EcoRI and probed with tammar wallaby SOX3. (PDF 2102 kb)

Supplementary Figure 2

DAPI inverted karyotype of male platypus taken from a male cell. (PDF 278 kb)

Supplementary Figure 3

Amino-acid sequence alignment of platypus DMRT1 with DMRT1 from different species. (PDF 106 kb)

Supplementary Table 1

Chromosome paints derived from elements of the translocation chain. (DOC 20 kb)

Supplementary Table 2

a, Alternate segregation of E-odd and E-even elements of the chain. b, Co-segregation of E-odd elements. (DOC 24 kb)

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Grützner, F., Rens, W., Tsend-Ayush, E. et al. In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432, 913–917 (2004). https://doi.org/10.1038/nature03021

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