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

Journal name:
Nature
Volume:
466,
Pages:
612–616
Date published:
DOI:
doi:10.1038/nature09172
Received
Accepted
Published online

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.

At a glance

Figures

  1. The Z amplicon.
    Figure 1: The Z amplicon.

    a. Fluorescence in situ hybridization (FISH) of Z-amplicon bacterial artificial chromosome (BAC) CH261-77N6 (red) to the distal long arm of the Z chromosome (blue). DAPI, 4′,6-diamidino-2-phenylindole. b, The Z amplicon (red) constitutes the most distal 11Mb of the Z chromosome. c, Triangular dot plots each comparing the sequence of a Z-chromosome BAC with itself. Within the plot, each dot represents a perfect match of 50 base pairs (bp). Direct repeats appear as horizontal lines. On the left, BAC CH261-73L15 contains six tandem repeats covering 120kb immediately proximal to the Z amplicon. On the right, BAC CH261-137P21, a representative Z-amplicon clone. Each 25–30-kb repeat unit is ~95% similar to any other, though some units have been disrupted by insertions and deletions. d, Genes in repeat units of the Z amplicon. Each 20-kb repeat unit of small array in CH261-73L15 contains one copy of ADCY10Z. Each 25–30kb repeat unit of Z amplicon contains one copy each of C2Orf3Z, MRPL19Z, and RICSZ. e, Reverse transcriptase (RT)–PCR analysis of Z-amplicon gene expression in adult tissues. HPRT1 is widely expressed in adult tissues and serves as positive control for reverse transcriptase reaction. All Z-amplicon genes are expressed in testis, but not other tissues.

  2. Independent origin of chicken Z and human X chromosomes.
    Figure 2: Independent origin of chicken Z and human X chromosomes.

    Rectangular dot plots show chromosomal locations of Z-orthologous or X-orthologous genes in other species. a, Chicken Z chromosome versus selected human chromosomes. The chicken Z chromosome is not orthologous to the human X chromosome, but is orthologous to portions of human autosomes 5 (yellow), 9 (blue) and 18 (purple). At right: three-colour projection of dot plots onto a unified schematic of the chicken Z chromosome, showing that orthology to human chromosomes 5, 9 and 18 accounts for most of the Z chromosome, with the exception of the Z amplicon on the distal long arm. b, Human X chromosome versus selected chicken chromosomes. The human X chromosome is not orthologous to the chicken Z chromosome, but is orthologous to portions of chicken autosomes 1 (red) and 4 (cyan). At right: two-colour projection of dot plots onto a unified schematic of the human X chromosome, showing that orthology to chicken chromosomes 1 and 4 spans the X chromosome. c, Chicken Z chromosome (orange) and human X chromosome (green) versus selected stickleback chromosomes. Chicken Z and human X orthologues occupy separate and distinct locations within the stickleback genome. Chicken Z orthologues are present on stickleback chromosomes 13 and 14, whereas human X orthologues are present on stickleback chromosomes 1, 4, 7 and 16. At bottom: two-colour projection of dot plots onto unified schematics of stickleback chromosomes, showing the relative contribution of chicken Z and human X orthologues.

  3. Convergent gene gain on the chicken Z and human X chromosomes.
    Figure 3: Convergent gene gain on the chicken Z and human X chromosomes.

    a, Gene density of Z and X chromosomes compared with autosomes. Both are unusually gene poor, with about half the gene density of a typical autosome. b, Venn diagrams comparing gene content of chicken Z and human X chromosomes with orthologous autosomes. Most genes on orthologous autosomes remain on the sex chromosomes; few have been lost. Both the chicken Z chromosome and the human X chromosome gained hundreds of genes not present on orthologous autosomes. c, Percentage of protein coding genes with testis ESTs in Unigene. On left: in comparison with chicken autosomes, the Z chromosome is enriched for testis-expressed genes. Single-copy Z chromosome genes (SC) show no enrichment for testis ESTs relative to autosomal genes, but nearly all multicopy (MC) genes are expressed in testis. On right: similar results obtain on the human X chromosome.

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Author information

Affiliations

  1. Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, Massachusetts 02142, USA

    • Daniel W. Bellott,
    • Helen Skaletsky,
    • Tatyana Pyntikova,
    • Laura G. Brown,
    • Steve Rozen &
    • David C. Page
  2. The Genome Center, Washington University School of Medicine, 4444 Forest Park Boulevard, St Louis, Missouri 63108, USA

    • Elaine R. Mardis,
    • Tina Graves,
    • Colin Kremitzki,
    • Wesley C. Warren &
    • Richard K. Wilson

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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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Supplementary information

PDF files

  1. Supplementary Information (25.3M)

    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.

Comments

  1. Report this comment #11982

    Robert Stonjek said:

    I hope we are not forgetting that monotremes have some 11 sex chromosomes including some similar to the X, Y, W and Z sex chromosomes as found in birds and mammals?

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