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Nat Ecol Evol. 2019 May;3(5):834-844. doi: 10.1038/s41559-019-0850-1. Epub 2019 Apr 1.

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

Xu L1,2, Auer G2, Peona V3, Suh A3, Deng Y4,5, Feng S4,5, Zhang G4,6,7, Blom MPK8,9, Christidis L10,11, Prost S12,13, Irestedt M14, Zhou Q15,16.

Author information

1
MOE Laboratory of Biosystems Homeostasis & Protection, Life Sciences Institute, Zhejiang University, Hangzhou, China.
2
Department of Molecular Evolution and Development, University of Vienna, Vienna, Austria.
3
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
4
China National Genebank, BGI-Shenzhen, Shenzhen, China.
5
BGI-Shenzhen, Shenzhen, China.
6
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
7
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
8
Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden.
9
Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany.
10
National Marin Science Centre, Southern Cross University, Coffs Harbour, New South Wales, Australia.
11
School of BioSciences, University of Melbourne, Parkville, Victoria, Australia.
12
Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, USA.
13
LOEWE-Center for Translational Biodiversity Genomics, Senckenberg, Frankfurt, Germany.
14
Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden. Martin.Irestedt@nrm.se.
15
MOE Laboratory of Biosystems Homeostasis & Protection, Life Sciences Institute, Zhejiang University, Hangzhou, China. zhouqi1982@zju.edu.cn.
16
Department of Molecular Evolution and Development, University of Vienna, Vienna, Austria. zhouqi1982@zju.edu.cn.

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.

PMID:
30936435
DOI:
10.1038/s41559-019-0850-1
[Indexed for MEDLINE]

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