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Low conservation of gene content in the Drosophila Y chromosome

Nature volume 456, pages 949–951 (2008)Cite this article

Abstract

Chromosomal organization is sufficiently evolutionarily stable that large syntenic blocks of genes can be recognized even between species as distantly related as mammals and puffer fish (450 million years (Myr) of divergence)1,2,3,4,5,6,7. In Diptera, the gene content of the X chromosome and the autosomes is well conserved: in Drosophila more than 95% of the genes have remained on the same chromosome arm in the 12 sequenced species (63 Myr of divergence, traversing 400 Myr of evolution)2,4,6, and the same linkage groups are clearly recognizable in mosquito genomes (260 Myr of divergence)3,5,7. Here we investigate the conservation of Y-linked gene content among the 12 sequenced Drosophila species. We found that only a quarter of the Drosophila melanogaster Y-linked genes (3 out of 12) are Y-linked in all sequenced species, and that most of them (7 out of 12) were acquired less than 63 Myr ago. Hence, whereas the organization of other Drosophila chromosomes traces back to the common ancestor with mosquitoes, the gene content of the D. melanogaster Y chromosome is much younger. Gene losses are known to have an important role in the evolution of Y chromosomes8,9,10, and we indeed found two such cases. However, the rate of gene gain in the Drosophila Y chromosomes investigated is 10.9 times higher than the rate of gene loss (95% confidence interval: 2.3–52.5), indicating a clear tendency of the Y chromosomes to increase in gene content. In contrast with the mammalian Y chromosome, gene gains have a prominent role in the evolution of the Drosophila Y chromosome.

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Figure 1: Synteny analysis of the kl-5 gene.
Figure 2: Gene movements in the Drosophila Y chromosome.
Figure 3: Posterior density of the net rate of Y-linked gene gain in the Drosophila phylogeny.

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References

  1. Aparicio, S. et al. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes . Science 297, 1301–1310 (2002)

    Article  ADS  CAS  Google Scholar 

  2. Beverley, S. M. & Wilson, A. C. Molecular evolution in Drosophila and the higher diptera II. A time scale for fly evolution. J. Mol. Evol. 21, 1–13 (1984)

    Article  ADS  CAS  Google Scholar 

  3. Zdobnov, E. M. et al. Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster . Science 298, 149–159 (2002)

    Article  ADS  CAS  Google Scholar 

  4. Tamura, K., Subramanian, S. & Kumar, S. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21, 36–44 (2004)

    Article  CAS  Google Scholar 

  5. Yeates, D. K. & Wiegmann, B. M. The Evolutionary Biology of Flies 35 (Columbia Univ. Press, 2005)

    Google Scholar 

  6. Bhutkar, A., Russo, S. M., Smith, T. F. & Gelbart, W. M. Genome-scale analysis of positionally relocated genes. Genome Res. 17, 1880–1887 (2007)

    Article  CAS  Google Scholar 

  7. Nene, V. et al. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316, 1718–1723 (2007)

    Article  ADS  CAS  Google Scholar 

  8. Rice, W. R. Evolution of the Y sex chromosome in animals. Bioscience 46, 331–343 (1996)

    Article  Google Scholar 

  9. Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B 355, 1563–1572 (2000)

    Article  CAS  Google Scholar 

  10. Bachtrog, D., Hom, E., Wong, K. M., Maside, X. & de Jong, P. Genomic degradation of a young Y chromosome in Drosophila miranda . Genome Biol. 9, R30 (2008)

    Article  Google Scholar 

  11. Carvalho, A. B. et al. Y chromosome and other heterochromatic sequences of the Drosophila melanogaster genome: how far can we go? Genetica 117, 227–237 (2003)

    Article  CAS  Google Scholar 

  12. Hoskins, R. A. et al. Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316, 1625–1628 (2007)

    Article  ADS  CAS  Google Scholar 

  13. Ashburner, M., Golic, K. G. & Hawley, R. S. Drosophila: a Laboratory Handbook 2nd edn 607–639 (Cold Spring Harbour Laboratory Press, 2005)

    Google Scholar 

  14. Kennison, J. A. The genetic and cytological organization of the Y chromosome of Drosophila melanogaster . Genetics 98, 529–548 (1981)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Hackstein, J. H. & Hochstenbach, R. The elusive fertility genes of Drosophila: the ultimate haven for selfish genetic elements. Trends Genet. 11, 195–200 (1995)

    Article  CAS  Google Scholar 

  16. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837 (2003)

    Article  ADS  CAS  Google Scholar 

  17. Sturtevant, A. H. & Novitski, E. The homologies of the chromosome elements in the genus Drosophila . Genetics 26, 517–541 (1941)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Gepner, J. & Hays, T. S. A fertility region on the Y chromosome of Drosophila melanogaster encodes a dynein microtubule motor. Proc. Natl Acad. Sci. USA 90, 11132–11136 (1993)

    Article  ADS  CAS  Google Scholar 

  19. Carvalho, A. B., Lazzaro, B. P. & Clark, A. G. Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. Proc. Natl Acad. Sci. USA 97, 13239–13244 (2000)

    Article  ADS  CAS  Google Scholar 

  20. Carvalho, A. B., Dobo, B. A., Vibranovski, M. D. & Clark, A. G. Identification of five new genes on the Y chromosome of Drosophila melanogaster . Proc. Natl Acad. Sci. USA 98, 13225–13230 (2001)

    Article  ADS  CAS  Google Scholar 

  21. Carvalho, A. B. & Clark, A. G. Birth of a new gene on the Drosophila Y chromosome. The 44th Annual Drosophila Research Conference, Philadelphia, USA. Abstract 318C, page 113 (The Genetics Society of America, 2003)

    Google Scholar 

  22. Vibranovski, M. D., Koerich, L. B. & Carvalho, A. B. Two new Y-linked genes in Drosophila melanogaster . Genetics 179, 2325–2327 (2008)

    Article  CAS  Google Scholar 

  23. Carvalho, A. B. & Clark, A. G. Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307, 108–110 (2005)

    Article  ADS  CAS  Google Scholar 

  24. Drosophila 12 Genomes Consortium Evolution of genes and genomes on the Drosophila phylogeny. Nature 450, 203–218 (2007)

  25. Betran, E., Thornton, K. & Long, M. Retroposed new genes out of the X in Drosophila . Genome Res. 12, 1854–1859 (2002)

    Article  CAS  Google Scholar 

  26. Emerson, J. J., Kaessmann, H., Betran, E. & Long, M. Extensive gene traffic on the mammalian X chromosome. Science 303, 537–540 (2004)

    Article  ADS  CAS  Google Scholar 

  27. Sturgill, D., Zhang, Y., Parisi, M. & Oliver, B. Demasculinization of X chromosomes in the Drosophila genus. Nature 450, 238–241 (2007)

    Article  ADS  CAS  Google Scholar 

  28. Graves, J. A. Sex chromosome specialization and degeneration in mammals. Cell 124, 901–914 (2006)

    Article  Google Scholar 

  29. Murphy, W. J. et al. Novel gene acquisition on carnivore Y chromosomes. PLoS Genet. 2, e43 (2006)

    Article  Google Scholar 

  30. Hurst, L. D. Is Stellate a relict meiotic driver? Genetics 130, 229–230 (1992)

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank S. Kumar, P. O’Grady, T. Markow, A. J. Bhutkar, S. C. Vaz, E. Betran, A. A. Peixoto, P. H. Krieger and P. Paiva for comments on the manuscript and/or for sharing their unpublished results. We also thank T. Pinhão, A. Bastos and F. Krsticevic for help with the experiments, K. Krishnamoorthy for statistical advice and M. Fetchko for help with GenBank submission. This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq, Coordenação de Aperfeiçoamento do Pessoal de Ensino Superior-CAPES, FAPERJ, FIC-NIH grant TW007604-02 (A.B.C.) and NIH grant GM64590 (A.G.C.).

Author information

Authors and Affiliations

  1. Departamento de Genética, Universidade Federal do Rio de Janeiro, Caixa Postal 68011, CEP 21944-970, Rio de Janeiro, Brazil,

    Leonardo B. Koerich & Antonio Bernardo Carvalho

  2. Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA,

    Xiaoyun Wang & Andrew G. Clark

Authors
  1. Leonardo B. Koerich
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  2. Xiaoyun Wang
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  4. Antonio Bernardo Carvalho
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Correspondence to Antonio Bernardo Carvalho.

Supplementary information

Supplementary Information

This file contains Supplementary Discussions, Supplementary Methods, Supplementary Figures 1-11 with Legends, Supplementary Tables 1-5, Supplementary References and Supplementary Notes. (PDF 2733 kb)

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Koerich, L., Wang, X., Clark, A. et al. Low conservation of gene content in the Drosophila Y chromosome. Nature 456, 949–951 (2008). https://doi.org/10.1038/nature07463

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