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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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).
The authors declare no competing financial interests.
Integrated supplementary information
(a,f,k) Images of chicken Z–W lampbrush bivalents in phase contrast, oriented with the terminal giant lumpy (TGL) loops and the W chromosome at the top and the Z chromosome at the bottom. Scale bar, 10 μm. (b,g,l) FISH localization of BAC probes (red) on the same lampbrush chromosomes counterstained with DAPI (blue). (c–e,h–j,m–o) Magnification showing the DAPI-intense chromomeres of the W chromosome (c,h,m), the BAC hybridization signal (d,i,n), and the merged image (e,j,o). Chomomere 1 is furthest from the chiasma, and chromomere 7 is adjacent to the chiasma. CH261-75N4 localizes to chromomere 2 (b,e), CH261-107E4 localizes to chromomere 4 (g, j), and CH261-114G22 localizes to chromomere 7 (l,o).
Dot plots of nucleotide sequence identity in a window size of 50 bp and a step size of 1 bp. (a) Rectangular dot plot showing nucleotide identity between the most distal clones from the short arms of the W and Z chromosomes. The pseudoautosomal region of the Z and W chromosomes begins in telomeric repeats near the TCF4 gene. (b) Triangular dot plot showing nucleotide identity on the W chromosome in the 100 kb adjacent to the HINTW array. Two copies of HINTW are tandemly repeated outside the array.
Violin plots marked with the median (black circle) and interquartile range (black bar) comparing the annotations of the human orthologs of ancestral Z–W gene pairs identified in chicken (dark pink); 4 species (chicken, collared flycatcher, crested ibis, and emu) (medium pink); and all 14 published female avian genomes (light pink) versus the human orthologs of the remainder of ancestral Z genes (light yellow). P values obtained using one-tailed Mann–Whitney U tests are reported with the associated test statistic, U. (a) The human orthologs of ancestral Z–W pairs are more broadly expressed in adult human tissues than other ancestral Z genes. Chicken Z–W pairs n = 26, other ancestral Z genes n = 516, P < 1.6 × 10–3, U = 9,012; 4 species Z–W pairs n = 70, other ancestral Z genes n = 472, P < 0.047, U = 18,563; 14 species Z–W pairs n = 133, other ancestral Z genes n = 409, P < 0.13, U = 28,960. (b) The human orthologs of ancestral Z–W pairs are more highly expressed in human blastocysts than other ancestral Z genes. Chicken Z–W pairs n = 26, other ancestral Z genes n = 495, P < 5.4 × 10–5, U = 9,333; 4 species Z–W pairs n = 68, other ancestral Z genes n = 453, P < 0.087, U = 18,156; 14 species Z–W pairs n = 129, other ancestral Z genes n = 392, P < 0.011, U = 28,720.
Supplementary Figures 1–3 (PDF 541 kb)
Tiling path accessions and coordinates. (XLSX 59 kb)
Ancestral Z genes and associated statistics. (XLSX 295 kb)
Ancestral ZW pairs from all 14 species. (XLSX 90 kb)
GO term enrichment. (XLSX 41 kb)
FASTA sequence of the chicken W chromosome assembly. (TXT 6913 kb)
FASTA sequence of transcripts of chicken Z–W gene pairs. (TXT 20 kb)
FASTA-formatted alignment of chicken Z–W gene pairs and human orthologs. (TXT 158 kb)
Radiation hybrid mapping data. (TXT 175 kb)
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Bellott, D., Skaletsky, H., Cho, TJ. et al. Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators. Nat Genet 49, 387–394 (2017). https://doi.org/10.1038/ng.3778
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