Abstract

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.

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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 (https://db.cngb.org/cnsa;​ 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 (https://github.com/lurebgi/BOPsexChr).

Additional information

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

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Acknowledgements

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

Affiliations

  1. MOE Laboratory of Biosystems Homeostasis & Protection, Life Sciences Institute, Zhejiang University, Hangzhou, China

    • Luohao Xu
    •  & Qi Zhou
  2. Department of Molecular Evolution and Development, University of Vienna, Vienna, Austria

    • Luohao Xu
    • , Gabriel Auer
    •  & Qi Zhou
  3. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden

    • Valentina Peona
    •  & Alexander Suh
  4. China National Genebank, BGI-Shenzhen, Shenzhen, China

    • Yuan Deng
    • , Shaohong Feng
    •  & Guojie Zhang
  5. BGI-Shenzhen, Shenzhen, China

    • Yuan Deng
    •  & Shaohong Feng
  6. State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    • Guojie Zhang
  7. Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark

    • Guojie Zhang
  8. Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden

    • Mozes P. K. Blom
    •  & Martin Irestedt
  9. Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany

    • Mozes P. K. Blom
  10. National Marin Science Centre, Southern Cross University, Coffs Harbour, New South Wales, Australia

    • Les Christidis
  11. School of BioSciences, University of Melbourne, Parkville, Victoria, Australia

    • Les Christidis
  12. Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, USA

    • Stefan Prost
  13. LOEWE-Center for Translational Biodiversity Genomics, Senckenberg, Frankfurt, Germany

    • Stefan Prost

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Contributions

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.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Martin Irestedt or Qi Zhou.

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https://doi.org/10.1038/s41559-019-0850-1