Skip to main content
Genetics logoLink to Genetics
. 2004 Apr;166(4):1887–1895. doi: 10.1534/genetics.166.4.1887

Evolution of DMY, a newly emergent male sex-determination gene of medaka fish.

Jianzhi Zhang 1
PMCID: PMC1470821  PMID: 15126406

Abstract

The Japanese medaka fish Oryzias latipes has an XX/XY sex-determination system. The Y-linked sex-determination gene DMY is a duplicate of the autosomal gene DMRT1, which encodes a DM-domain-containing transcriptional factor. DMY appears to have originated recently within Oryzias, allowing a detailed evolutionary study of the initial steps that led to the new gene and new sex-determination system. Here I analyze the publicly available DMRT1 and DMY gene sequences of Oryzias species and report the following findings. First, the synonymous substitution rate in DMY is 1.73 times that in DMRT1, consistent with the male-driven evolution hypothesis. Second, the ratio of the rate of nonsynonymous nucleotide substitution (d(N)) to that of synonymous substitution (d(S)) is significantly higher in DMY than in DMRT1. Third, in DMRT1, the d(N)/d(S) ratio for the DM domain is lower than that for non-DM regions, as expected from the functional importance of the DM domain. But in DMY, the opposite is observed and the DM domain is likely under positive Darwinian selection. Fourth, only one characteristic amino acid distinguishes all DMY sequences from all DMRT1 sequences, suggesting that a single amino acid change may be largely responsible for the establishment of DMY as the male sex-determination gene in medaka fish.

Full Text

The Full Text of this article is available as a PDF (241.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Berta P., Hawkins J. R., Sinclair A. H., Taylor A., Griffiths B. L., Goodfellow P. N., Fellous M. Genetic evidence equating SRY and the testis-determining factor. Nature. 1990 Nov 29;348(6300):448–450. doi: 10.1038/348448A0. [DOI] [PubMed] [Google Scholar]
  2. Bohossian H. B., Skaletsky H., Page D. C. Unexpectedly similar rates of nucleotide substitution found in male and female hominids. Nature. 2000 Aug 10;406(6796):622–625. doi: 10.1038/35020557. [DOI] [PubMed] [Google Scholar]
  3. Carmichael A. N., Fridolfsson A. K., Halverson J., Ellegren H. Male-biased mutation rates revealed from Z and W chromosome-linked ATP synthase alpha-subunit (ATP5A1) sequences in birds. J Mol Evol. 2000 May;50(5):443–447. doi: 10.1007/s002390010046. [DOI] [PubMed] [Google Scholar]
  4. Chang B. H., Shimmin L. C., Shyue S. K., Hewett-Emmett D., Li W. H. Weak male-driven molecular evolution in rodents. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):827–831. doi: 10.1073/pnas.91.2.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Charlesworth B., Charlesworth D. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 2000 Nov 29;355(1403):1563–1572. doi: 10.1098/rstb.2000.0717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ellegren H., Fridolfsson A. K. Male-driven evolution of DNA sequences in birds. Nat Genet. 1997 Oct;17(2):182–184. doi: 10.1038/ng1097-182. [DOI] [PubMed] [Google Scholar]
  7. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
  8. Foster J. W., Brennan F. E., Hampikian G. K., Goodfellow P. N., Sinclair A. H., Lovell-Badge R., Selwood L., Renfree M. B., Cooper D. W., Graves J. A. Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature. 1992 Oct 8;359(6395):531–533. doi: 10.1038/359531a0. [DOI] [PubMed] [Google Scholar]
  9. Foster J. W., Graves J. A. An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1927–1931. doi: 10.1073/pnas.91.5.1927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Just W., Rau W., Vogel W., Akhverdian M., Fredga K., Graves J. A., Lyapunova E. Absence of Sry in species of the vole Ellobius. Nat Genet. 1995 Oct;11(2):117–118. doi: 10.1038/ng1095-117. [DOI] [PubMed] [Google Scholar]
  11. Kahn N. W., Quinn T. W. Male-driven evolution among Eoaves? A test of the replicative division hypothesis in a heterogametic female (ZW) system. J Mol Evol. 1999 Dec;49(6):750–759. doi: 10.1007/pl00006597. [DOI] [PubMed] [Google Scholar]
  12. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  13. Kondo Mariko, Nanda Indrajit, Hornung Ute, Asakawa Shuichi, Shimizu Nobuyoshi, Mitani Hiroshi, Schmid Michael, Shima Akihiro, Schartl Manfred. Absence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr Biol. 2003 Mar 4;13(5):416–420. doi: 10.1016/s0960-9822(03)00125-8. [DOI] [PubMed] [Google Scholar]
  14. Kumar S., Hedges S. B. A molecular timescale for vertebrate evolution. Nature. 1998 Apr 30;392(6679):917–920. doi: 10.1038/31927. [DOI] [PubMed] [Google Scholar]
  15. Kumar S., Tamura K., Jakobsen I. B., Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001 Dec;17(12):1244–1245. doi: 10.1093/bioinformatics/17.12.1244. [DOI] [PubMed] [Google Scholar]
  16. Li Wen Hsiung, Yi Soojin, Makova Kateryna. Male-driven evolution. Curr Opin Genet Dev. 2002 Dec;12(6):650–656. doi: 10.1016/s0959-437x(02)00354-4. [DOI] [PubMed] [Google Scholar]
  17. Matsuda Masaru, Nagahama Yoshitaka, Shinomiya Ai, Sato Tadashi, Matsuda Chika, Kobayashi Tohru, Morrey Craig E., Shibata Naoki, Asakawa Shuichi, Shimizu Nobuyoshi. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 2002 May 12;417(6888):559–563. doi: 10.1038/nature751. [DOI] [PubMed] [Google Scholar]
  18. Matsuda Masaru, Sato Tadashi, Toyazaki Yota, Nagahama Yoshitaka, Hamaguchi Satoshi, Sakaizumi Mitsuru. Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes. Zoolog Sci. 2003 Feb;20(2):159–161. doi: 10.2108/zsj.20.159. [DOI] [PubMed] [Google Scholar]
  19. McVean G. T., Hurst L. D. Evidence for a selectively favourable reduction in the mutation rate of the X chromosome. Nature. 1997 Mar 27;386(6623):388–392. doi: 10.1038/386388a0. [DOI] [PubMed] [Google Scholar]
  20. Miyata T., Hayashida H., Kuma K., Mitsuyasu K., Yasunaga T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol. 1987;52:863–867. doi: 10.1101/sqb.1987.052.01.094. [DOI] [PubMed] [Google Scholar]
  21. Nachman M. W., Crowell S. L. Estimate of the mutation rate per nucleotide in humans. Genetics. 2000 Sep;156(1):297–304. doi: 10.1093/genetics/156.1.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nanda Indrajit, Hornung Ute, Kondo Mariko, Schmid Michael, Schartl Manfred. Common spontaneous sex-reversed XX males of the medaka Oryzias latipes. Genetics. 2003 Jan;163(1):245–251. doi: 10.1093/genetics/163.1.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nanda Indrajit, Kondo Mariko, Hornung Ute, Asakawa Shuichi, Winkler Christoph, Shimizu Atsushi, Shan Zhihong, Haaf Thomas, Shimizu Nobuyoshi, Shima Akihiro. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A. 2002 Aug 22;99(18):11778–11783. doi: 10.1073/pnas.182314699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oohara I., Sawano K., Okazaki T. Mitochondrial DNA sequence analysis of the masu salmon--phylogeny in the genus Oncorhynchus. Mol Phylogenet Evol. 1997 Feb;7(1):71–78. doi: 10.1006/mpev.1996.0373. [DOI] [PubMed] [Google Scholar]
  25. Pamilo P., O'Neill R. J. Evolution of the Sry genes. Mol Biol Evol. 1997 Jan;14(1):49–55. doi: 10.1093/oxfordjournals.molbev.a025701. [DOI] [PubMed] [Google Scholar]
  26. Rzhetsky A., Kumar S., Nei M. Four-cluster analysis: a simple method to test phylogenetic hypotheses. Mol Biol Evol. 1995 Jan;12(1):163–167. doi: 10.1093/oxfordjournals.molbev.a040185. [DOI] [PubMed] [Google Scholar]
  27. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  28. Shimmin L. C., Chang B. H., Li W. H. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. doi: 10.1038/362745a0. [DOI] [PubMed] [Google Scholar]
  29. Sinclair A. H., Berta P., Palmer M. S., Hawkins J. R., Griffiths B. L., Smith M. J., Foster J. W., Frischauf A. M., Lovell-Badge R., Goodfellow P. N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature. 1990 Jul 19;346(6281):240–244. doi: 10.1038/346240a0. [DOI] [PubMed] [Google Scholar]
  30. Souer E., van Houwelingen A., Kloos D., Mol J., Koes R. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell. 1996 Apr 19;85(2):159–170. doi: 10.1016/s0092-8674(00)81093-4. [DOI] [PubMed] [Google Scholar]
  31. Stevanović M., Lovell-Badge R., Collignon J., Goodfellow P. N. SOX3 is an X-linked gene related to SRY. Hum Mol Genet. 1993 Dec;2(12):2013–2018. doi: 10.1093/hmg/2.12.2013. [DOI] [PubMed] [Google Scholar]
  32. Sutton K. A., Wilkinson M. F. Rapid evolution of a homeodomain: evidence for positive selection. J Mol Evol. 1997 Dec;45(6):579–588. doi: 10.1007/pl00006262. [DOI] [PubMed] [Google Scholar]
  33. Suzuki Y., Nei M. Reliabilities of parsimony-based and likelihood-based methods for detecting positive selection at single amino acid sites. Mol Biol Evol. 2001 Dec;18(12):2179–2185. doi: 10.1093/oxfordjournals.molbev.a003764. [DOI] [PubMed] [Google Scholar]
  34. Suzuki Yoshiyuki, Nei Masatoshi. Simulation study of the reliability and robustness of the statistical methods for detecting positive selection at single amino acid sites. Mol Biol Evol. 2002 Nov;19(11):1865–1869. doi: 10.1093/oxfordjournals.molbev.a004010. [DOI] [PubMed] [Google Scholar]
  35. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ting C. T., Tsaur S. C., Wu M. L., Wu C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998 Nov 20;282(5393):1501–1504. doi: 10.1126/science.282.5393.1501. [DOI] [PubMed] [Google Scholar]
  37. Tucker P. K., Lundrigan B. L. Rapid evolution of the sex determining locus in Old World mice and rats. Nature. 1993 Aug 19;364(6439):715–717. doi: 10.1038/364715a0. [DOI] [PubMed] [Google Scholar]
  38. Tucker Priscilla K., Adkins Ronald M., Rest Joshua S. Differential rates of evolution for the ZFY-related zinc finger genes, Zfy, Zfx, and Zfa in the mouse genus Mus. Mol Biol Evol. 2003 Apr 25;20(6):999–1005. doi: 10.1093/molbev/msg112. [DOI] [PubMed] [Google Scholar]
  39. Whitfield L. S., Lovell-Badge R., Goodfellow P. N. Rapid sequence evolution of the mammalian sex-determining gene SRY. Nature. 1993 Aug 19;364(6439):713–715. doi: 10.1038/364713a0. [DOI] [PubMed] [Google Scholar]
  40. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 1998 May;15(5):568–573. doi: 10.1093/oxfordjournals.molbev.a025957. [DOI] [PubMed] [Google Scholar]
  41. Yang Z., Nielsen R., Goldman N., Pedersen A. M. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 2000 May;155(1):431–449. doi: 10.1093/genetics/155.1.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zarkower D. Establishing sexual dimorphism: conservation amidst diversity? Nat Rev Genet. 2001 Mar;2(3):175–185. doi: 10.1038/35056032. [DOI] [PubMed] [Google Scholar]
  43. Zhang J., Kumar S., Nei M. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol. 1997 Dec;14(12):1335–1338. doi: 10.1093/oxfordjournals.molbev.a025743. [DOI] [PubMed] [Google Scholar]
  44. Zhang J., Nei M. Accuracies of ancestral amino acid sequences inferred by the parsimony, likelihood, and distance methods. J Mol Evol. 1997;44 (Suppl 1):S139–S146. doi: 10.1007/pl00000067. [DOI] [PubMed] [Google Scholar]
  45. Zhang J., Nei M. Evolution of Antennapedia-class homeobox genes. Genetics. 1996 Jan;142(1):295–303. doi: 10.1093/genetics/142.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zhang J., Rosenberg H. F., Nei M. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3708–3713. doi: 10.1073/pnas.95.7.3708. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES