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

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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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 (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).

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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.

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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.

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Correspondence to Martin Irestedt or Qi Zhou.

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

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