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

Monotreme sex chromosomes – implications for the evolution of amniote sex chromosomes

Paul D. Waters A B and Jennifer A. Marshall Graves A
+ Author Affiliations
- Author Affiliations

A Comparative Genomics Group, Research School of Biological Sciences, School of Biology, The Australian National University, GPO Box 475, Canberra, ACT 2601, Australia.

B Corresponding author. Email: paul.waters@anu.edu.au

Reproduction, Fertility and Development 21(8) 943-951 https://doi.org/10.1071/RD09250
Submitted: 5 May 2009  Accepted: 13 July 2009   Published: 30 October 2009

Abstract

In vertebrates, a highly conserved pathway of genetic events controls male and female development, to the extent that many genes involved in human sex determination are also involved in fish sex determination. Surprisingly, the master switch to this pathway, which intuitively could be considered the most critical step, is inconsistent between vertebrate taxa. Interspersed in the vertebrate tree there are species that determine sex by environmental cues such as the temperature at which eggs are incubated, and then there are genetic sex-determination systems, with male heterogametic species (XY systems) and female heterogametic species (ZW systems), some of which have heteromorphic, and others homomorphic, sex chromosomes. This plasticity of sex-determining switches in vertebrates has made tracking the events of sex chromosome evolution in amniotes a daunting task, but comparative gene mapping is beginning to reveal some striking similarities across even distant taxa. In particular, the recent completion of the platypus genome sequence has completely changed our understanding of when the therian mammal X and Y chromosomes first arose (they are up to 150 million years younger than previously thought) and has also revealed the unexpected insight that sex determination of the amniote ancestor might have been controlled by a bird-like ZW system.


References

Alsop, A. E. , Miethke, P. , Rofe, R. , Koina, E. , Sankovic, N. , Deakin, J. E. , Haines, H. , Rapkins, R. W. , and Graves, J. A. M. (2005). Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosome Res. 13, 627–636.
Crossref | GoogleScholarGoogle Scholar | PubMed | Ohno S. (1967). ‘Sex Chromosomes and Sex-linked Genes.’ (Springer-Verlag: New York.)

Page, J. , Berrios, S. , Rufas, J. S. , Parra, M. T. , Sija, J. A. , Heyting, C. , and Fernandez-Donosoo, R. (2003). The meiotic pairing of X and Y chromosomes in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements. J. Cell Sci. 116, 551–560.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Page, J. , Berrios, S. , Parra, M. T. , Viera, A. , Suja, J. A. , Prieto, I. , Barbero, J. L. , Rufas, J. S. , and Fernandez-Donoso, R. (2005). The program of sex chromosome pairing in meiosis is highly conserved across marsupial species: implications for sex chromosome evolution. Genetics 170, 793–799.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pask, A. , Renfree, M. B. , and Graves, J. A. M. (2000). The human sex-reversing ATRX gene has a homologue on the marsupial Y chromosome, ATRY: implications for the evolution of mammalian sex determination. Proc. Natl Acad. Sci. USA 97, 13198–13202.
Crossref | GoogleScholarGoogle Scholar |

Pokorná, M. , and Kratochvíl, L. (2009). Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool. J. Linn. Soc. 156, 168–183.
Crossref | GoogleScholarGoogle Scholar |

Quinn, A. E. , Georges, A. , Sarre, S. D. , Guarino, F. , Ezaz, T. , and Graves, J. A. M. (2007). Temperature sex reversal implies sex gene dosage in a reptile. Science 316, 411.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Radder, R. S. , Quinn, A. E. , Georges, A. , Sarre, S. D. , and Shine, R. (2008). Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol. Lett. 4, 176–178.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rahn, M. I. , and Solari, A. J. (1986). Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet. Cell Genet. 43, 187–193.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Raudsepp, T. , Lee, E. J. , Kata, S. R. , Brinkmeyer, C. , Mickelson, J. R. , Skow, L. C. , Womack, J. E. , and Chowdhary, B. P. (2004). Exceptional conservation of horse–human gene order on X chromosome revealed by high-resolution radiation hybrid mapping. Proc. Natl Acad. Sci. USA 101, 2386–2391.
Crossref | GoogleScholarGoogle Scholar |

Rens, W. , Grützner, F. , O’Brien, P. C. , Fairclough, H. , Graves, J. A. M. , and Ferguson-Smith, M. A. (2004). Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution. Proc. Natl Acad. Sci. USA 101, 16 257–16 261.
Crossref | GoogleScholarGoogle Scholar |

Rens, W. , O’Brien, P. C. , Grützner, F. , Clarke, O. , and Graphodatskaya, D. , et al. (2007). The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z. Genome Biol. 8, R243.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Rodríguez Delgado, C. L. , Waters, P. D. , Gilbert, C. , Robinson, T. J. , and Graves, J. A. M. (2009). Physical mapping of the elephant X chromosome: conservation of gene order over 105 years. Chromosome Res. ,
Crossref | GoogleScholarGoogle Scholar |

Ross, M. T. , Grafham, D. V. , Coffey, A. J. , Scherer, S. , and McLay, K. , et al. (2005). The DNA sequence of the human X chromosome. Nature 434, 325–337.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Schmid, M. , Nanda, I. , Guttenbach, M. , Steinlein, C. , and Hoehn, M. , et al. (2000). First report on Chicken Genes and Chromosomes 2000. Cytogenet. Cell Genet. 90, 169–218.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Sekido, R. , and Lovell-Badge, R. (2009). Sex determination and SRY: down to a wink and a nudge? Trends Genet. 25, 19–29.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shetty, S. , Griffin, D. K. , and Graves, J. A. M. (1999). Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res. 7, 289–295.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Shetty, S. , Kirby, P. , Zarkower, D. , and Graves, J. A. M. (2002). DMRT1 in a ratite bird: evidence for a role in sex determination and discovery of a putative regulatory element. Cytogenet. Genome Res. 99, 245–251.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Skaletsky, H. , Kuroda-Kawaguchi, T. , Minx, P. J. , Cordum, H. S. , and Hillier, L. , et al. (2003). The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Smith, C. A. , McClive, P. J. , Western, P. S. , Reed, K. J. , and Sinclair, A. H. (1999). Conservation of a sex-determining gene. Nature 402, 601–602.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Solari, A. J. , and Bianchi, N. O. (1975). The synaptic behaviour of the X and Y chromosomes in the marsupial Monodelphis dimidiata. Chromosoma 52, 11–25.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Spencer, J. A. , Sinclair, A. H. , Watson, J. M. , and Graves, J. A. M. (1991). Genes on the short arm of the human X chromosome are not shared with the marsupial X. Genomics 11, 339–345.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Toder, R. , Wakefield, M. J. , and Graves, J. A. M. (2000). The minimal mammalian Y chromosome – the marsupial Y as a model system. Cytogenet. Cell Genet. 91, 285–292.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Veyrunes, F. , Waters, P. D. , Miethke, P. , Rens, W. , and McMillan, D. , et al. (2008). Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965–973.
Crossref | GoogleScholarGoogle Scholar | PubMed |

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

Waters, P. D. , Duffy, B. , Frost, C. J. , Delbridge, M. L. , and Graves, J. A. M. (2001). The human Y chromosome derives largely from a single autosomal region added to the sex chromosomes 80–130 million years ago. Cytogenet. Cell Genet. 92, 74–79.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Waters, P. D. , Delbridge, M. L. , Deakin, J. E. , El-Mogharbel, N. , Kirby, P. J. , Carvalho-Silva, D. R. , and Graves, J. A. M. (2005). Autosomal location of genes from the conserved mammalian X in the platypus (Ornithorhynchus anatinus): implications for mammalian sex chromosome evolution. Chromosome Res. 13(4), 401–410.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Waters, P. D. , Wallis, M. C. , and Graves, J. A. M. (2007). Mammalian sex-origin and evolution of the Y chromosome and SRY. Semin. Cell Dev. Biol. 18, 389–400.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Watson, J. M. , Spencer, J. A. , Riggs, A. D. , and Graves, J. A. M. (1990). The X chromosome of monotremes shares a highly conserved region with the eutherian and marsupial X chromosomes despite the absence of X chromosome inactivation. Proc. Natl Acad. Sci. USA 87, 7125–7129.
Crossref | GoogleScholarGoogle Scholar |

Wrigley, J. M. , and Graves, J. A. M. (1988). Sex chromosome homology and incomplete, tissue-specific X-inactivation suggest that monotremes represent an intermediate stage of mammalian sex chromosome evolution. J. Hered. 79, 115–118.
PubMed |

Yoshimoto, S. , Okada, E. , Umemoto, H. , Tamura, K. , Uno, Y. , Nishida-Umehara, C. , Matsuda, Y. , Takamatsu, N. , Shiba, T. , and Ito, M. (2008). A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc. Natl Acad. Sci. USA 105, 2469–2474.
Crossref | GoogleScholarGoogle Scholar |

Zhang, P. , Zhou, H. , Chen, Y. Q. , Liu, Y. F. , and Qu, L. H. (2005). Mitogenomic perspectives on the origin and phylogeny of living amphibians. Syst. Biol. 54, 391–400.
Crossref | GoogleScholarGoogle Scholar | PubMed |