Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Reduced adaptation of a non-recombining neo-Y chromosome

Abstract

Sex chromosomes are generally believed to have descended from a pair of homologous autosomes. Suppression of recombination between the ancestral sex chromosomes led to the genetic degeneration of the Y chromosome1. In response, the X chromosome may become dosage-compensated1,2. Most proposed mechanisms for the degeneration of Y chromosomes involve the rapid fixation of deleterious mutations on the Y1. Alternatively, Y-chromosome degeneration might be a response to a slower rate of adaptive evolution, caused by its lack of recombination3. Here we report patterns of DNA polymorphism and divergence at four genes located on the neo-sex chromosomes of Drosophila miranda. We show that a higher rate of protein sequence evolution of the neo-X-linked copy of Cyclin B relative to the neo-Y copy is driven by positive selection, which is consistent with the adaptive hypothesis for the evolution of the Y chromosome3. In contrast, the neo-Y-linked copies of even-skipped and roundabout show an elevated rate of protein evolution relative to their neo-X homologues, probably reflecting the reduced effectiveness of selection against deleterious mutations in a non-recombining genome1. Our results provide evidence for the importance of sexual recombination for increasing and maintaining the level of adaptation of a population.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Phylogenetic relationships between the species investigated, constructed from the coding region of CycB.
Figure 2: Plots of the relative values of the log-likelihood functions ln L(kV), ln L(kS) and ln L(kV, ΔS) as a function of k, the reduction in the effective population size of the neo-Y chromosome relative to the neo-X.

References

  1. Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B 55, 1563–1572 (2000).

    Article  Google Scholar 

  2. Marin, I., Siegal, M. L. & Baker, B. S. The evolution of dosage-compensation mechanisms. BioEssays 22, 1106–1114 (2000).

    CAS  Article  PubMed  Google Scholar 

  3. Orr, H. A. & Kim, Y. An adaptive hypothesis for the evolution of the Y chromosome. Genetics 150, 1693–1698 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Lahn, B. T., Pearson, N. M. & Jegalian, K. The human Y chromosome, in the light of evolution. Nature Rev. Genet. 2, 207–216 (2001).

    CAS  Article  PubMed  Google Scholar 

  5. 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).

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Powell, J. R. Progress and Prospects in Evolutionary Biology: The Drosophila Model (Oxford Univ. Press, New York, 1997).

    Google Scholar 

  7. Schaeffer, S. W. & Miller, E. L. Molecular population genetics of an electrophoretically monomorphic protein in the alcohol dehydrogenase region of Drosophila pseudoobscura. Genetics 132, 163–178 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Gethmann, R. C. Crossing over in males of higher Diptera (Brachycera). J. Hered. 79, 344–350 (1988).

    Article  PubMed  Google Scholar 

  9. Steinemann, M. & Steinemann, S. Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica 102–103, 409–420 (1998).

    Article  PubMed  Google Scholar 

  10. Waters, P. D., Duffy, B., Frost, C. J., Delbridge, M. L. & Graves, J. A. 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 (2001).

    CAS  Article  PubMed  Google Scholar 

  11. Das, M., Mutsuddi, D., Duttagupta, A. K. & Mukherjee, A. S. Segmental heterogeneity in replication and transcription of the X2 chromosome of Drosophila miranda and conservativeness in the evolution of dosage compensation. Chromosoma 87, 373–388 (1982).

    CAS  Article  Google Scholar 

  12. Li, W. Molecular Evolution (Sinauer Associates, Sunderland, Massachusetts, 1997).

    Google Scholar 

  13. Yi, S. & Charlesworth, B. Contrasting patterns of molecular evolution of the genes on the new and old sex chromosomes of Drosophila miranda. Mol. Biol. Evol. 17, 703–717 (2000).

    CAS  Article  PubMed  Google Scholar 

  14. Wang, R. L. & Hey, J. The speciation history of Drosophila pseudoobscura and close relatives: inferences from DNA sequence variation at the period locus. Genetics 144, 1113–1126 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).

    Book  Google Scholar 

  16. Wright, S. Evolution and the Genetics of Populations (Univ. of Chicago Press, Chicago, 1969).

    Google Scholar 

  17. Bachtrog, D. & Charlesworth, B. Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda. Curr. Biol. 10, 1025–1031 (2000).

    CAS  Article  PubMed  Google Scholar 

  18. Filatov, D. A., Moneger, F., Negrutiu, I. & Charlesworth, D. Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature 404, 388–390 (2000).

    ADS  CAS  Article  PubMed  Google Scholar 

  19. Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997).

    CAS  PubMed  Google Scholar 

  20. McDonald, J. H. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).

    ADS  CAS  Article  PubMed  Google Scholar 

  21. Barton, N. H. Genetic hitchhiking. Phil. Trans. R. Soc. Lond. B 355, 1553–1562 (2000).

    CAS  Article  Google Scholar 

  22. Hudson, R. R., Kreitman, M. & Aguade, M. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Lynch, M. & Blanchard, J. L. Deleterious mutation accumulation in organelle genomes. Genetica 102–103, 29–39 (1998).

    Article  PubMed  Google Scholar 

  24. Fridolfsson, A. K. & Ellegren, H. Molecular evolution of the avian CHD1 genes on the Z and W sex chromosomes. Genetics 155, 1903–1912 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Maynard Smith, J. The Evolution of Sex (Cambridge Univ. Press, Cambridge, 1978).

    Google Scholar 

  26. Barton, N. H. & Charlesworth, B. Why sex and recombination? Science 281, 1986–1990 (1998).

    CAS  Article  PubMed  Google Scholar 

  27. Bell, G. The Masterpiece of Nature (Univ. of California, Berkeley, 1982).

    Google Scholar 

  28. Tajima, F. Statistical analysis of DNA polymorphism. Jpn J. Genet. 68, 567–595 (1993).

    CAS  Article  PubMed  Google Scholar 

  29. Hudson, R. R. in Oxford Surveys in Evolutionary Biology Vol. 7 (eds Futuyma, D. & Antonovics, J.) 1–44 (Oxford Univ. Press, Oxford, 1990).

    Google Scholar 

  30. Weiss, G. & von Haeseler, A. Inference of population history using a likelihood approach. Genetics 149, 1539–1546 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank P. Andolfatto, N. Barton, D. Charlesworth, I. Gordo, P. Keightley and S. Wright for helpful comments on the manuscript. D.B. is supported by a Marie Curie fellowship and B.C. by the Royal Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Doris Bachtrog.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bachtrog, D., Charlesworth, B. Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416, 323–326 (2002). https://doi.org/10.1038/416323a

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/416323a

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing