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Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition

Abstract

In birds, as in mammals, one pair of chromosomes differs between the sexes. In birds, males are ZZ and females ZW. In mammals, males are XY and females XX. Like the mammalian XY pair, the avian ZW pair is believed to have evolved from autosomes, with most change occurring in the chromosomes found in only one sex—the W and Y chromosomes1,2,3,4,5. By contrast, the sex chromosomes found in both sexes—the Z and X chromosomes—are assumed to have diverged little from their autosomal progenitors2. Here we report findings that challenge this assumption for both the chicken Z chromosome and the human X chromosome. The chicken Z chromosome, which we sequenced essentially to completion, is less gene-dense than chicken autosomes but contains a massive tandem array containing hundreds of duplicated genes expressed in testes. A comprehensive comparison of the chicken Z chromosome with the finished sequence of the human X chromosome demonstrates that each evolved independently from different portions of the ancestral genome. Despite this independence, the chicken Z and human X chromosomes share features that distinguish them from autosomes: the acquisition and amplification of testis-expressed genes, and a low gene density resulting from an expansion of intergenic regions. These features were not present on the autosomes from which the Z and X chromosomes originated but were instead acquired during the evolution of Z and X as sex chromosomes. We conclude that the avian Z and mammalian X chromosomes followed convergent evolutionary trajectories, despite their evolving with opposite (female versus male) systems of heterogamety. More broadly, in birds and mammals, sex chromosome evolution involved not only gene loss in sex-specific chromosomes, but also marked expansion and gene acquisition in sex chromosomes common to males and females.

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Figure 1: The Z amplicon.
Figure 2: Independent origin of chicken Z and human X chromosomes.
Figure 3: Convergent gene gain on the chicken Z and human X chromosomes.

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Data deposits

Predicted Z-amplicon transcript sequences and the complete assembled sequence of the Z chromosome are available at http://jura.wi.mit.edu/page/papers/Bellott_et_al_2010/ (see Supplementary Table 5 for GenBank accession numbers).

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Acknowledgements

We thank E. Rapoport for technical assistance, S. Repping and S. van Daalen for experimental advice, and E. Anderson, T. Endo, M. Gill, A. Hochwagen, C. Hongay, Y. Hu, J. Hughes, J. Marszalek, J. Mueller and Y. Soh for comments on the manuscript. We thank the Broad Institute Genome Sequencing Platform and Genome Sequencing and Analysis Program, F. Di Palma and K. Lindblad-Toh for making the unpublished data for Gasterosteus aculeatus available. This work was supported by the National Institutes of Health and the Howard Hughes Medical Institute.

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Contributions

D.W.B., H.S., W.C.W., S.R., R.K.W. and D.C.P. planned the project. D.W.B. and L.G.B. performed BAC mapping. D.W.B. performed RT–PCR analysis. T.G. and C.K. were responsible for finished BAC sequencing. D.W.B. and H.S. performed comparative sequence analyses. T.P. performed FISH analysis. E.R.M. performed 454 sequencing. D.W.B. and D.C.P. wrote the paper.

Corresponding author

Correspondence to David C. Page.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-12 with legends (please note that Supplementary Figure 1 spans 24 pages), Supplementary Tables 1-5 and Supplementary Notes 1, which gives additional information about Supplementary Figure 12. (PDF 25983 kb)

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Bellott, D., Skaletsky, H., Pyntikova, T. et al. Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466, 612–616 (2010). https://doi.org/10.1038/nature09172

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