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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
REVIEW

The enigma of the platypus genome

Wesley C. Warren A C and Frank Grützner B
+ Author Affiliations
- Author Affiliations

A The Genome Center, Washington University School of Medicine, 4444 Forest Park Boulevard, St Louis, MO 63108, USA.

B School of Molecular & Biomedical Science, The University of Adelaide, Adelaide, SA 5005, Australia.

C Corresponding author. Email: wwarren@watson.wustl.edu

Australian Journal of Zoology 57(4) 157-165 https://doi.org/10.1071/ZO09051
Submitted: 21 April 2009  Accepted: 7 August 2009   Published: 26 October 2009

Abstract

Over two centuries after the first platypus specimen stirred the scientific community in Europe, the whole-genome sequence of the duck-billed platypus has been completed and is publicly available. After publication of eutherian and marsupial genomes, this is the first genome of a monotreme filling an important evolutionary gap between the divergence of birds more that 300 million years ago and marsupials more than 140 million years ago. Monotremes represent the most basal surviving branch of mammals and the platypus genome sequence allows unprecedented insights into the evolution of mammals and the fascinating biology of the egg-laying mammals. Here, we discuss some of the key findings of the analysis of the platypus genome and point to new findings and future research directions, which illustrate the broad impact of the platypus genome project for understanding monotreme biology and mammalian genome evolution.


Acknowledgements

We thank Dr Marilyn Renfree and Dr Russell Jones for helpful comments and Dr Geoff Shaw for the use of the animal silhouettes used in Fig. 1.


References

Akiyama S. (1998). Molecular ecology of the platypus (Ornithorhynchus anatinus). Ph.D. Thesis, La Trobe University, Melbourne.

Alfaro, M. E. , Santini, F. , Brock, C. , Alamillo, H. , Dornburg, A. , Rabosky, D. L. , Carnevale, G. , and Harmon, L. J. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences of the USA 106(32), 13 410–13 414.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Darwin C. (1859). ‘The Origin of Species by means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life.’ (John Murray: London.)

de Plater, G. , Martin, R. , and Milburn, P. (1998). A C-type natriuretic peptide from the venom of the platypus (Ornithorhyncus anatinus): structure and pharmacology. Comparative Biochemistry and Physiology. C. Comparative Pharmacology and Toxicology 120, 99–110.
Crossref | GoogleScholarGoogle Scholar | CAS | Gemmell N. J. (1994). Population and evolutionary investigations on the platypus (Ornithorhynchus anatinus). Ph.D. Thesis, La Trobe University, Melbourne.

Grant T. (2007). ‘Platypus.’ 4th edn. (CSIRO Publishing: Melbourne.)

Gregory, J. E. , Iggo, A. , McIntyre, A. K. , and Proske, U. (1989). Responses of electroreceptors in the snout of the echidna. The Journal of Physiology 414, 521–538.
CAS | PubMed | Griffiths M. (1978). ‘The Biology of the Monotremes.’ (Academic Press: New York, San Fransisco, London.)

Grützner, F. , Rens, W. , Tsend-Ayush, E. , El-Mogharbel, N. , O’Brien, P. C. , Jones, R. C. , Ferguson-Smith, M. A. , and Graves, J. A. M. (2004). In the platypus a meiotic chain of ten sex chromosomes shares genes with the bird Z and mammal X chromosomes. Nature 432, 913–917.
Crossref | GoogleScholarGoogle Scholar | PubMed | Jørgensen J. M. (2006). Morphology of electroreceptive sensory organs. In ‘Springer Handbook of Auditory Research (Book Series), Vol. 21’. (Eds T. H. Bullock, C. D. Hopkins, A. N. Popper and R. R. Fay.) pp. 47–67. (Springer: New York.)

Killian, J. K. , Byrd, J. C. , Jirtle, J. V. , Munday, B. L. , Stoskopf, M. K. , MacDonald, R. G. , and Jirtle, R. L. (2000). M6P/IGF2R imprinting evolution in mammals. Molecular Cell 5, 707–716.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Madsen O. (2009). Mammmals (Mammalia). In ‘The Timetree of Life’. (Eds S. B. Hedges and S. Kumar.) pp. 459–461. (Oxford University Press: Oxford.)

Moore, T. , and Haig, D. (1991). Genomic imprinting in mammalian development: a parental tug-of-war. Trends in Genetics 7, 45–49.
CAS | PubMed | Moyal A. (2001). ‘Platypus.’ (Allen & Unwin: Sydney.)

Murtagh, C. , and Sharman, G. B. (2009). Monotreme chromosomes: an introductory review. Australian Journal of Zoology 57, 149–155.
Crossref | GoogleScholarGoogle Scholar | Springer M. S. , and Krajewski C. W. (2009). Monotremes (Prototheria). In ‘The Timetree of Life’. (Eds S. B. Hedges and S. Kumar.) pp. 462–465. (Oxford University Press: Oxford.)

Suzuki, S. , Ono, R. , Narita, T. , Pask, A. J. , and Shaw, G., , et al. (2007). Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLOS Genetics 3, e55.
Crossref | GoogleScholarGoogle Scholar | PubMed | Temple-Smith P. D. (1973). Seasonal breeding biology of the platypus, Ornithorhynchus anatinus (Shaw, 1799), with special reference to the male. Ph.D. Thesis, Australian National University, Canberra.

Torres, A. , et al. (1999). Solution structure of a defensin-like peptide from platypus venom. The Biochemical Journal 341, 785–794.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Tsend-Ayush, E. , Lim, S. Y. , Pask, A. J. , Hamdan, D. D. M. , Renfree, M. B. , and Grützner, F. (2009). Characterisation of ATRX, DMRT1, DMRT7 and WT1 in the platypus (Ornithorhynchus anatinus). Reproduction, Fertility and Development 21, 985–991.
Crossref | GoogleScholarGoogle Scholar |

Vanpe´, C. , Buschiazzo, E. , Abdelkrim, J. , Morrow, G. , Nicol, S. , and Gemmell, N. J. (2009). Development of microsatellite markers for the short-beaked echidna using three different approaches. Australian Journal of Zoology 57, 219–223.
Crossref | GoogleScholarGoogle Scholar |

van Rheede, T. , Bastiaans, T. , Boone, D. N. , Hedges, S. B. , de Jong, W. W. , and Madsen, O. (2006). The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and therians. Molecular Biology and Evolution 23, 587–597.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Veyrunes, F. , Waters, P. D. , Miethke, P. , Rens, W. , McMillan, D. , and Alsop, A. E. , Grützner, F. , Deakin, J. E. , Whittington, C. M. , Schatzkamer, K. , Kremitzki, C. L. , Graves, T. , Ferguson-Smith, M. A. , Warren, W. , and Graves, J. A. M. (2008). Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Research 18, 965–973.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Warren, W. C. , Hillier, L. W. , Graves, J. A. M. , Birney, E. , and Ponting, C. P. , et al. (2008). Genome analysis of platypus reveals unique signatures of evolution. Nature 453, 175–183.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Waters, P. D. , and Graves, J. A. M. (2009). Monotreme sex chromosomes – implications for the evolution of amniote sex chromosomes. Reproduction, Fertility and Development 57, 943–951.
Crossref | GoogleScholarGoogle Scholar |

Whittington, C. M. , et al. (2008). Defensins and the convergent evolution of platypus and reptile venom genes. Genome Research 18, 986–994.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Whittington, C. M. , Koh, J. M. , Warren, W. C. , Papenfuss, A. T. , and Torres, A. M. , Kuchel, P. W. , and Belov, K. (2009). Understanding and utilising mammalian venom via a platypus venom transcriptome. Journal of Proteomics 72, 155–164.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Wildman, D. E. , Chen, C. , Erez, O. , Grossman, L. I. , Goodman, M. , and Romero, R. (2006). Evolution of the mammalian placenta revealed by phylogenetic analysis. Proceedings of the National Academy of Sciences of the United States of America 103, 3203–3208.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Woodburne, M. O. , Rich, T. H. , and Springer, M. S. (2003). The evolution of tribospheny and the antiquity of mammalian clades. Molecular Phylogenetics and Evolution 28(2), 360–385.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Wong, E. S. W. , Papenfuss, A. T. , Miller, R. D. , and Belov, K. (2009). Hatching time for monotreme immunology. Australian Journal of Zoology 57, 185–198.
Crossref | GoogleScholarGoogle Scholar |

Zakon, H. H. , Lu, Y. , Zwickl, D. J. , and Hillis, D. M. (2006). Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proceedings of the National Academy of Sciences of the United States of America 103, 3675–3680.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Zakon, H. H. , Zwickl, D. J. , Lu, Y. , and Hillis, D. M. (2008). Molecular evolution of communication signals in electric fish. The Journal of Experimental Biology 211, 1814–1818.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |