Abstract

After birds diverged from mammals, different ancestral autosomes evolved into sex chromosomes in each lineage. In birds, females are ZW and males are ZZ, but in mammals females are XX and males are XY. We sequenced the chicken W chromosome, compared its gene content with our reconstruction of the ancestral autosomes, and followed the evolutionary trajectory of ancestral W-linked genes across birds. Avian W chromosomes evolved in parallel with mammalian Y chromosomes, preserving ancestral genes through selection to maintain the dosage of broadly expressed regulators of key cellular processes. We propose that, like the human Y chromosome, the chicken W chromosome is essential for embryonic viability of the heterogametic sex. Unlike other sequenced sex chromosomes, the chicken W chromosome did not acquire and amplify genes specifically expressed in reproductive tissues. We speculate that the pressures that drive the acquisition of reproduction-related genes on sex chromosomes may be specific to the male germ line.

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Accessions

Primary accessions

BioProject

NCBI Reference Sequence

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Acknowledgements

We thank M. Delany (University of California, Davis) for UCD001 DNA, A. Vignal and M. Morrison (INRA Toulouse) for ChickRH6 radiation hybrid panel DNA, M. Lovett (Washington University, St. Louis) for chicken embryonic fibroblasts, C. Friedman and B. Trask for flow-sorted chicken W chromosomes, F. McCarthy for permission to use the Chickspress RNA–seq data set (PRJNA204941), and the “Chromas” Saint-Petersburg University Resource Center and L. Rapoport for technical assistance. This work was supported by the National Institutes of Health and the Howard Hughes Medical Institute. S.G. and E.G. were supported by the Russian Foundation of Basic Research (grant 16-04-01823a).

Author information

Affiliations

  1. Whitehead Institute, Cambridge, Massachusetts, USA.

    • Daniel W Bellott
    • , Helen Skaletsky
    • , Ting-Jan Cho
    • , Laura Brown
    • , Tatyana Pyntikova
    • , Natalia Koutseva
    •  & David C Page
  2. Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Daniel W Bellott
    •  & David C Page
  3. Howard Hughes Medical Institute, Whitehead Institute, Cambridge, Massachusetts, USA.

    • Helen Skaletsky
    • , Laura Brown
    •  & David C Page
  4. McDonnell Genome Institute, Washington University School of Medicine, St. Louis, Missouri, USA.

    • Devin Locke
    • , Tina Graves
    • , Colin Kremitzki
    • , Wesley C Warren
    •  & Richard K Wilson
  5. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, USA.

    • Nancy Chen
    •  & Andrew G Clark
  6. Cornell Laboratory of Ornithology, Ithaca, New York, USA.

    • Nancy Chen
  7. Department of Evolution and Ecology, University of California, Davis, Davis, California, USA.

    • Nancy Chen
  8. Saint Petersburg State University, Saint Petersburg, Russian Federation.

    • Svetlana Galkina
    •  & Elena Gaginskaya
  9. Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, USA.

    • Andrew G Clark

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Contributions

D.W.B., H.S., W.C.W., A.G.C., E.G., R.K.W., and D.C.P. planned the project. D.W.B., H.S., T.-J.C., D.L., and N.C. developed female-specific sequence-tagged sites. D.W.B., H.S., T.-J.C., and L.B. performed clone mapping. D.W.B., T.-J.C., N.K., T.G., and C.K. performed clone sequencing. S.G. and T.P. performed FISH analyses. D.W.B. and T.-J.C. performed RH mapping. D.W.B. and H.S. performed sequence analyses. D.W.B. and D.C.P. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to David C Page.

Integrated supplementary information

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–3

Excel files

  1. 1.

    Supplementary Table 1

    Tiling path accessions and coordinates.

  2. 2.

    Supplementary Table 2

    Ancestral Z genes and associated statistics.

  3. 3.

    Supplementary Table 3

    Ancestral ZW pairs from all 14 species.

  4. 4.

    Supplementary Table 4

    GO term enrichment.

Text files

  1. 1.

    Supplementary Data 1

    FASTA sequence of the chicken W chromosome assembly.

  2. 2.

    Supplementary Data 2

    FASTA sequence of transcripts of chicken Z–W gene pairs.

  3. 3.

    Supplementary Data 3

    FASTA-formatted alignment of chicken Z–W gene pairs and human orthologs.

  4. 4.

    Supplementary Data 4

    Radiation hybrid mapping data.

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DOI

https://doi.org/10.1038/ng.3778

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