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How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals

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Abstract

The duck-billed platypus is an extraordinary mammal. Its chromosome complement is no less extraordinary, for it includes a system in which ten sex chromosomes form an extensive meiotic chain in males. Such meiotic multiples are unprecedented in vertebrates but occur sporadically in plant and invertebrate species. In this paper, we review the evolution and formation of meiotic multiples in plants and invertebrates to try to gain insights into the origin of the platypus meiotic multiple. We describe the meiotic hurdles that translocated mammalian chromosomes face, which make longer chains disadvantageous in mammals, and we discuss how sex chromosomes and dosage compensation might have affected the evolution of sex-linked meiotic multiples. We conclude that the evolutionary conservation of the chain in monotremes, the structural properties of the translocated chromosomes and the highly accurate segregation at meiosis make the platypus system remarkably different from meiotic multiples in other species. We discuss alternative evolutionary models, which fall broadly into two categories: either the chain is the result of a sequence of translocation events from an ancestral pair of sex chromosomes (Model I) or the entire chain came into being at once by hybridization of two populations with different chromosomal rearrangements sharing monobrachial homology (Model II).

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Acknowledgements

We are grateful to W. Rens, P.C.M. O’Brien and M.A. Ferguson-Smith for generating and providing platypus whole chromosome paints and to W. Rens and two anonymous reviewers for helpful comments on the manuscript. F.G. and J.A.M.G. acknowledge funding from the Australian Research Council.

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  1. Frank Gruetzner

    Present address: School of Molecular and Biomedical Science, University of Adelaide, Adelaide, SA, 5005, Australia

Authors and Affiliations

  1. Research School of Biological Sciences, Australian National University, Canberra, ACT, 2601, Australia

    Frank Gruetzner & Jennifer A. Marshall Graves

  2. Department of Genetics, Yale University School of Medicine, New Haven, CT, USA

    Terry Ashley

  3. School of Botany and Zoology, Australian National University, Canberra, ACT, 2601, Australia

    David M. Rowell

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  1. Frank Gruetzner
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  2. Terry Ashley
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Correspondence to Frank Gruetzner.

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Communicated by E.A. Nigg

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Gruetzner, F., Ashley, T., Rowell, D.M. et al. How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals. Chromosoma 115, 75–88 (2006). https://doi.org/10.1007/s00412-005-0034-4

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