Skip to main content

Thank you for visiting 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.

Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds


Songbirds have a species number close to that of mammals and are classic models for studying speciation and sexual selection. Sex chromosomes are hotspots of both processes, yet their evolutionary history in songbirds remains unclear. We characterized genomes of 11 songbird species, with 5 genomes of bird-of-paradise species. We conclude that songbird sex chromosomes have undergone four periods of recombination suppression before species radiation, producing a gradient of pairwise sequence divergence termed ‘evolutionary strata’. The latest stratum was probably due to a songbird-specific burst of retrotransposon CR1–E1 elements at its boundary, instead of the chromosome inversion generally assumed for suppressing sex-linked recombination. The formation of evolutionary strata has reshaped the genomic architecture of both sex chromosomes. We find stepwise variations of Z-linked inversions, repeat and guanine–cytosine (GC) contents, as well as W-linked gene loss rate associated with the age of strata. A few W-linked genes have been preserved for their essential functions, indicated by higher and broader expression of lizard orthologues compared with those of other sex-linked genes. We also find a different degree of accelerated evolution of Z-linked genes versus autosomal genes among species, potentially reflecting diversified intensity of sexual selection. Our results uncover the dynamic evolutionary history of songbird sex chromosomes and provide insights into the mechanisms of recombination suppression.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: The Z and W chromosomes of different songbirds.
Fig. 2: Evolutionary strata of songbirds.
Fig. 3: Fast-Z evolution of songbirds.
Fig. 4: The W-linked genes are preserved by purifying selection.
Fig. 5: Comparison of gene loss between W chromosomes of songbirds and Y chromosomes of primates.

Data availability

Genome sequencing and RNA-seq data generated in this study have been deposited in the NCBI SRA under PRJNA491255. The raw genomic reads of Paradisaea raggiana are available in the CNGB Nucleotide Sequence Archive (;​ accession ​number CNP0000186). The genome assemblies are available under NCBI BioProject portal (PRJNA491255). The IDs of W-linked scaffolds are included in Supplementary Table 10.

Code availability

Custom scripts and pipelines used in this study have been deposited at Github (


  1. 1.

    World Bird List v.8.2 (IOC) (2018);

  2. 2.

    Barker, F. K., Cibois, A., Schikler, P., Feinstein, J. & Cracraft, J. Phylogeny and diversification of the largest avian radiation. Proc. Natl Acad. Sci. USA 101, 11040–11045 (2004).

    CAS  Google Scholar 

  3. 3.

    Ellegren, H. et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756–760 (2012).

    CAS  Google Scholar 

  4. 4.

    Poelstra, J. W. et al. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 1410–1414 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344–350 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 10474 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Mank, J. E. Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am. Nat. 173, 141–150 (2009).

    Google Scholar 

  8. 8.

    Coyne, J. A. Genetics and speciation. Nature 355, 511 (1992).

    CAS  Google Scholar 

  9. 9.

    Charlesworth, B., Coyne, J. & Barton, N. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130, 113–146 (1987).

    Google Scholar 

  10. 10.

    Smeds, L. et al. Evolutionary analysis of the female-specific avian W chromosome. Nat. Commun. 6, 7330 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Hooper, D. M. & Price, T. D. Chromosomal inversion differences correlate with range overlap in passerine birds. Nat. Ecol. Evol. 1, 1526–1534 (2017).

    Google Scholar 

  12. 12.

    Hooper, D. M. & Price, T. D. Rates of karyotypic evolution in Estrildid finches differ between island and continental clades. Evolution 69, 890–903 (2015).

    Google Scholar 

  13. 13.

    Backström, N. et al. A high-density scan of the Z chromosome in Ficedula flycatchers reveals candidate loci for diversifying selection. Evolution 64, 3461–3475 (2010).

    Google Scholar 

  14. 14.

    Elgvin, T. O. et al. Hybrid speciation in sparrows II: a role for sex chromosomes?. Mol. Ecol. 20, 3823–3837 (2011).

    CAS  Google Scholar 

  15. 15.

    Storchová, R., Reif, J. & Nachman, M. W. Female heterogamety and speciation: reduced introgression of the Z chromosome between two species of nightingales. Evolution 64, 456–471 (2010).

    Google Scholar 

  16. 16.

    Li, W. H., Yi, S. & Makova, K. Male-driven evolution. Curr. Opin. Genet. Dev. 12, 650–656 (2002).

    CAS  Google Scholar 

  17. 17.

    Wang, Z. et al. Temporal genomic evolution of bird sex chromosomes. BMC Evol. Biol. 14, 250 (2014).

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Ellegren, H. Characteristics, causes and evolutionary consequences of male-biased mutation. Proc. Biol. Sci. 274, 1–10 (2007).

    CAS  Google Scholar 

  19. 19.

    Smeds, L., Qvarnström, A. & Ellegren, H. Direct estimate of the rate of germline mutation in a bird. Genome Res. 26, 1211–1218 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Vicoso, B. & Charlesworth, B. Effective population size and the faster-X effect: an extended model. Evolution 63, 2413–2426 (2009).

    Google Scholar 

  21. 21.

    Mank, J. E., Nam, K. & Ellegren, H. Faster-Z evolution is predominantly due to genetic drift. Mol. Biol. Evol. 27, 661–670 (2010).

    CAS  Google Scholar 

  22. 22.

    Wright, A. E. et al. Variation in promiscuity and sexual selection drives avian rate of Faster-Z evolution. Mol. Ecol. 24, 1218–1235 (2015).

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Zhou, Q. et al. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346, 1246338 (2014).

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Bellott, D. W. et al. Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators. Nat. Genet. 49, 387–394 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Charlesworth, D., Charlesworth, B. & Marais, G. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95, 118–128 (2005).

    CAS  Google Scholar 

  26. 26.

    Bachtrog, D. Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat. Rev. Genet. 14, 113–124 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B 355, 1563–1572 (2000).

    CAS  Google Scholar 

  28. 28.

    Bachtrog, D. The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179, 1513–1525 (2008).

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Soh, Y. Q. et al. Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159, 800–813 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Bellott, D. W. et al. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508, 494–499 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Zhou, Q. & Bachtrog, D. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337, 341–345 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Koerich, L. B., Wang, X., Clark, A. G. & Carvalho, A. B. Low conservation of gene content in the Drosophila Y chromosome. Nature 456, 949–951 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Wright, A. E., Harrison, P. W., Montgomery, S. H., Pointer, M. A. & Mank, J. E. Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome. Evolution 68, 3281–3295 (2014).

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Moghadam, H. K., Pointer, M. A., Wright, A. E., Berlin, S. & Mank, J. E. W chromosome expression responds to female-specific selection. Proc. Natl Acad. Sci. USA 109, 8207–8211 (2012).

    CAS  Google Scholar 

  35. 35.

    Cortez, D. et al. Origins and functional evolution of Y chromosomes across mammals. Nature 508, 488–493 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Bergero, R., Forrest, A., Kamau, E. & Charlesworth, D. Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175, 1945–1954 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Gorelick, R. et al. Abrupt shortening of bird W chromosomes in ancestral Neognathae. Biol. J. Linn. Soc. Lond. 119, 488–496 (2016).

    Google Scholar 

  38. 38.

    Rice, W. R. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911–914 (1987).

    Google Scholar 

  39. 39.

    Claramunt, S. & Cracraft, J. A new time tree reveals Earth historys imprint on the evolution of modern birds. Sci. Adv. 1, e1501005–e1501005 (2015).

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Smeds, L. et al. Genomic identification and characterization of the pseudoautosomal region in highly differentiated avian sex chromosomes. Nat. Commun. 5, 5448 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Pala, I. et al. Evidence of a neo-sex chromosome in birds. Heredity 108, 264–272 (2012).

    CAS  Google Scholar 

  42. 42.

    Ross, M. T. et al. The DNA sequence of the human X chromosome. Nature 434, 325–337 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    O’Connor, R. E. et al. Chromosome-level assembly reveals extensive rearrangement in saker falcon and budgerigar, but not ostrich, genomes. Genome Biol. 19, 171 (2018).

    PubMed  PubMed Central  Google Scholar 

  44. 44.

    Wright, A. E., Dean, R., Zimmer, F. & Mank, J. E. How to make a sex chromosome. Nat. Commun. 7, 12087 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Duret, L. & Galtier, N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu. Rev. Genomics Hum. Genet. 10, 285–311 (2009).

    CAS  Google Scholar 

  46. 46.

    Kent, T. V., Uzunović, J. & Wright, S. I. Coevolution between transposable elements and recombination. Philos. Trans. R. Soc. B 372, 20160458 (2017).

    Google Scholar 

  47. 47.

    Suh, A. et al. Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat. Commun. 2, 443 (2011).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Friocourt, F. et al. Recurrent DCC gene losses during bird evolution. Sci. Rep. 7, 37569 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Patthey, C., Tong, Y. G., Tait, C. M. & Wilson, S. I. Evolution of the functionally conserved DCC gene in birds. Sci. Rep. 7, 42029 (2017).

    PubMed  PubMed Central  Google Scholar 

  50. 50.

    Ligon, R. A. et al. Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise. PLoS Biol. 16, e2006962 (2018).

    PubMed  PubMed Central  Google Scholar 

  51. 51.

    Irestedt, M., Jonsson, K. A., Fjeldsa, J., Christidis, L. & Ericson, P. G. An unexpectedly long history of sexual selection in birds-of-paradise. BMC Evol. Biol. 9, 235 (2009).

    PubMed  PubMed Central  Google Scholar 

  52. 52.

    Dunn, P. O., Whittingham, L. A. & Pitcher, T. E. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55, 161–175 (2001).

    CAS  Google Scholar 

  53. 53.

    Diamond, J. Biology of birds of paradise and bowerbirds. Annu. Rev. Ecol. Syst. 17, 17–37 (1986).

    Google Scholar 

  54. 54.

    Kirkpatrick, M. & Ryan, M. J. The evolution of mating preferences and the paradox of the lek. Nature 350, 33–38 (1991).

    Google Scholar 

  55. 55.

    Suh, A. The specific requirements for CR1 retrotransposition explain the scarcity of retrogenes in birds. J. Mol. Evol. 81, 18–20 (2015).

    CAS  Google Scholar 

  56. 56.

    Huang, N., Lee, I., Marcotte, E. M. & Hurles, M. E. Characterising and predicting haploinsufficiency in the human genome. PLoS Genet. 6, e1001154 (2010).

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Stock, M. et al. Ever-young sex chromosomes in European tree frogs. PLoS Biol. 9, e1001062 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Vicoso, B., Emerson, J. J., Zektser, Y., Mahajan, S. & Bachtrog, D. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11, e1001643 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Charlesworth, D. Evolution of recombination rates between sex chromosomes. Philos. Trans. R. Soc. Lond. B 372, 20160456 (2017).

    Google Scholar 

  60. 60.

    Lemaitre, C. et al. Footprints of inversions at present and past pseudoautosomal boundaries in human sex chromosomes. Genome Biol. Evol. 1, 56–66 (2009).

    PubMed  PubMed Central  Google Scholar 

  61. 61.

    Ellis, N. A. et al. The pseudoautosomal boundary in man is defined by an Alu repeat sequence inserted on the Y chromosome. Nature 337, 81–84 (1989).

    CAS  Google Scholar 

  62. 62.

    Raudsepp, T. & Chowdhary, B. P. The eutherian pseudoautosomal region. Cytogenet. Genome Res. 147, 81–94 (2015).

    Google Scholar 

  63. 63.

    Zamudio, N. et al. DNA methylation restrains transposons from adopting a chromatin signature permissive for meiotic recombination. Genes Dev. 29, 1256–1270 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Ben-Aroya, S., Mieczkowski, P. A., Petes, T. D. & Kupiec, M. The compact chromatin structure of a Ty repeated sequence suppresses recombination hotspot activity in Saccharomyces cerevisiae. Mol. Cell 15, 221–231 (2004).

    CAS  Google Scholar 

  65. 65.

    Knief, U. et al. Fitness consequences of polymorphic inversions in the zebra finch genome. Genome Biol. 17, 199 (2016).

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Campagna, L. et al. Repeated divergent selection on pigmentation genes in a rapid finch radiation. Sci. Adv. 3, e1602404 (2017).

    PubMed  PubMed Central  Google Scholar 

  67. 67.

    Irwin, D. E. Sex chromosomes and speciation in birds and other ZW systems. Mol. Ecol. 27, 3831–3851 (2018).

    CAS  Google Scholar 

  68. 68.

    Prost, S. et al. Comparative analyses identify genomic features potentially involved in the evolution of birds-of-paradise. GigaScience (2018).

  69. 69.

    Gnerre, S. et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA 108, 1513–1518 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1, 18 (2012).

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Cantarel, B. L. et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 18, 188–196 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).

    PubMed  PubMed Central  Google Scholar 

  73. 73.

    Stanke, M. & Waack, S. Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19, ii215–ii225 (2003).

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Marçais, G. et al. MUMmer4: A fast and versatile genome alignment system. PLoS Comput. Biol. 14, e1005944 (2018).

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Genomics (q-bio.GN) (2013).

  76. 76.

    Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Zhang, J., Li, C., Zhou, Q. & Zhang, G. Improving the ostrich genome assembly using optical mapping data. GigaScience 4, 24 (2015).

    PubMed  PubMed Central  Google Scholar 

  78. 78.

    Xu, L. et al. Evolutionary dynamics of sex chromosomes of palaeognathous birds. Preprint at bioRxiv (2018).

  79. 79.

    Harris, R. S. Improved pairwise alignment of genomic DNA. PhD thesis, The Pennsylvania State University (2017).

  80. 80.

    Kent, W. J. BLAT — the BLAST-like alignment tool. Genome Res. 12, 656–64 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Lechner, M. et al. Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12, 124 (2011).

    PubMed  PubMed Central  Google Scholar 

  83. 83.

    Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    CAS  Google Scholar 

  84. 84.

    Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS  Google Scholar 

  85. 85.

    Zhang, G. et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346, 1311–1320 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. 86.

    Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    CAS  Google Scholar 

  87. 87.

    Jiao, X. et al. DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics 28, 1805–1806 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Yanai, I. et al. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21, 650–659 (2005).

    CAS  Google Scholar 

  91. 91.

    del Hoyo, J, . & Elliot, A. & Sargatal, J. & Christie, D. & de Juana, E. Handbook of the Birds of the World Alive (Lynx Editions, 2019).

Download references


We thank the Smithsonian Institute (G. Graves), Australian National Wildlife Collection, CSIRO Sustainable Ecosystems (L. Joseph), Museum Victoria, Australia (J. Sumner), Division of Vertebrate Zoology Yale University, Peabody Museum of Natural History (K. Zyskowski) for tissue samples; and E. Scholes for discussions on BOP. We also acknowledge the support from Science for Life Laboratory, the National Genomics Infrastructure (NGI), Uppmax. L.X. is supported by the uni:docs fellowship programme from University of Vienna. M.I. is supported by the Swedish Research Council (grant no. 621-2014-5113). Q.Z. is supported by National Natural Science Foundation of China (grant nos. 31722050 and 31671319), the Fundamental Research Funds for the Central Universities (grant no. 2018XZZX002-04) and start-up funds from Zhejiang University. The computational analyses were performed on CUBE cluster from Department of Computational System Biology of University of Vienna and Vienna Scientific Cluster.

Author information




Q.Z. and M.I. conceived the project. L.X., Q.Z., G.A., V.P., Y.D., S.F., G.Z., M.B. and S. P. performed the analyses. Q.Z., L.X., A.S., L.C. and M.I. wrote the paper.

Corresponding authors

Correspondence to Martin Irestedt or Qi Zhou.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xu, L., Auer, G., Peona, V. et al. Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds. Nat Ecol Evol 3, 834–844 (2019).

Download citation


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