Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes

Frederick Veyrunes, Paul Waters, Pat Miethke, Willem Rens, Daniel McMillan, Amber Alsop, Frank Grutzner, Janine Deakin, Camilla Whittington, Kyriena Schatzkamer, Colin Kremitzki, Tina Graves, Malcolm Ferguson-Smith, Wes Warren, Jennifer Marshall Graves

Research output: Contribution to journalArticle

208 Citations (Scopus)

Abstract

In therian mammals (placentals and marsupials), sex is determined by an XX female: XY male system, in which a gene (SRY) on the Y affects male determination. There is no equivalent in other amniotes, although some taxa (notably birds and snakes) have differentiated sex chromosomes. Birds have a ZW female: ZZ male system with no homology with mammal sex chromosomes, in which dosage of a Z-borne gene (possibly DMRT1) affects male determination. As the most basal mammal group, the egg-laying monotremes are ideal for determining how the therian XY system evolved. The platypus has an extraordinary sex chromosome complex, in which five X and five Y chromosomes pair in a translocation chain of alternating X and Y chromosomes. We used physical mapping to identify genes on the pairing regions between adjacent X and Y chromosomes. Most significantly, comparative mapping shows that, contrary to earlier reports, there is no homology between the platypus and therian X chromosomes. Orthologs of genes in the conserved region of the human X (including SOX3, the gene from which SRY evolved) all map to platypus chromosome 6, which therefore represents the ancestral autosome from which the therian X and Y pair derived. Rather, the platypus X chromosomes have substantial homology with the bird Z chromosome (including DMRT1) and to segments syntenic with this region in the human genome. Thus, platypus sex chromosomes have strong homology with bird, but not to therian sex chromosomes, implying that the therian X and Y chromosomes (and the SRY gene) evolved from an autosomal pair after the ivergence of monotremes only 166 million years ago. Therefore, the therian X and Y are more than 145 million years younger than previously thought.
Original languageEnglish
Pages (from-to)965-973
Number of pages9
JournalGenome Research
Volume18
DOIs
Publication statusPublished - 2008
Externally publishedYes

Fingerprint

Platypus
Sex Chromosomes
X Chromosome
Birds
Mammals
Y Chromosome
Genes
Y-Linked Genes
Marsupialia
Chromosomes, Human, Pair 6
Snakes
Human Genome
Ovum
Chromosomes

Cite this

Veyrunes, F., Waters, P., Miethke, P., Rens, W., McMillan, D., Alsop, A., ... Marshall Graves, J. (2008). Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Research, 18, 965-973. https://doi.org/10.1101/gr.7101908
Veyrunes, Frederick ; Waters, Paul ; Miethke, Pat ; Rens, Willem ; McMillan, Daniel ; Alsop, Amber ; Grutzner, Frank ; Deakin, Janine ; Whittington, Camilla ; Schatzkamer, Kyriena ; Kremitzki, Colin ; Graves, Tina ; Ferguson-Smith, Malcolm ; Warren, Wes ; Marshall Graves, Jennifer. / Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. In: Genome Research. 2008 ; Vol. 18. pp. 965-973.
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abstract = "In therian mammals (placentals and marsupials), sex is determined by an XX female: XY male system, in which a gene (SRY) on the Y affects male determination. There is no equivalent in other amniotes, although some taxa (notably birds and snakes) have differentiated sex chromosomes. Birds have a ZW female: ZZ male system with no homology with mammal sex chromosomes, in which dosage of a Z-borne gene (possibly DMRT1) affects male determination. As the most basal mammal group, the egg-laying monotremes are ideal for determining how the therian XY system evolved. The platypus has an extraordinary sex chromosome complex, in which five X and five Y chromosomes pair in a translocation chain of alternating X and Y chromosomes. We used physical mapping to identify genes on the pairing regions between adjacent X and Y chromosomes. Most significantly, comparative mapping shows that, contrary to earlier reports, there is no homology between the platypus and therian X chromosomes. Orthologs of genes in the conserved region of the human X (including SOX3, the gene from which SRY evolved) all map to platypus chromosome 6, which therefore represents the ancestral autosome from which the therian X and Y pair derived. Rather, the platypus X chromosomes have substantial homology with the bird Z chromosome (including DMRT1) and to segments syntenic with this region in the human genome. Thus, platypus sex chromosomes have strong homology with bird, but not to therian sex chromosomes, implying that the therian X and Y chromosomes (and the SRY gene) evolved from an autosomal pair after the ivergence of monotremes only 166 million years ago. Therefore, the therian X and Y are more than 145 million years younger than previously thought.",
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Veyrunes, F, Waters, P, Miethke, P, Rens, W, McMillan, D, Alsop, A, Grutzner, F, Deakin, J, Whittington, C, Schatzkamer, K, Kremitzki, C, Graves, T, Ferguson-Smith, M, Warren, W & Marshall Graves, J 2008, 'Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes', Genome Research, vol. 18, pp. 965-973. https://doi.org/10.1101/gr.7101908

Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. / Veyrunes, Frederick; Waters, Paul; Miethke, Pat; Rens, Willem; McMillan, Daniel; Alsop, Amber; Grutzner, Frank; Deakin, Janine; Whittington, Camilla; Schatzkamer, Kyriena; Kremitzki, Colin; Graves, Tina; Ferguson-Smith, Malcolm; Warren, Wes; Marshall Graves, Jennifer.

In: Genome Research, Vol. 18, 2008, p. 965-973.

Research output: Contribution to journalArticle

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AU - Veyrunes, Frederick

AU - Waters, Paul

AU - Miethke, Pat

AU - Rens, Willem

AU - McMillan, Daniel

AU - Alsop, Amber

AU - Grutzner, Frank

AU - Deakin, Janine

AU - Whittington, Camilla

AU - Schatzkamer, Kyriena

AU - Kremitzki, Colin

AU - Graves, Tina

AU - Ferguson-Smith, Malcolm

AU - Warren, Wes

AU - Marshall Graves, Jennifer

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Veyrunes F, Waters P, Miethke P, Rens W, McMillan D, Alsop A et al. Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Research. 2008;18:965-973. https://doi.org/10.1101/gr.7101908