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Origins and functional evolution of Y chromosomes across mammals

Nature volume 508, pages 488493 (24 April 2014) | Download Citation

Abstract

Y chromosomes underlie sex determination in mammals, but their repeat-rich nature has hampered sequencing and associated evolutionary studies. Here we trace Y evolution across 15 representative mammals on the basis of high-throughput genome and transcriptome sequencing. We uncover three independent sex chromosome originations in mammals and birds (the outgroup). The original placental and marsupial (therian) Y, containing the sex-determining gene SRY, emerged in the therian ancestor approximately 180 million years ago, in parallel with the first of five monotreme Y chromosomes, carrying the probable sex-determining gene AMH. The avian W chromosome arose approximately 140 million years ago in the bird ancestor. The small Y/W gene repertoires, enriched in regulatory functions, were rapidly defined following stratification (recombination arrest) and erosion events and have remained considerably stable. Despite expression decreases in therians, Y/W genes show notable conservation of proto-sex chromosome expression patterns, although various Y genes evolved testis-specificities through differential regulatory decay. Thus, although some genes evolved novel functions through spatial/temporal expression shifts, most Y genes probably endured, at least initially, because of dosage constraints.

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Accessions

Primary accessions

Gene Expression Omnibus

Sequence Read Archive

Data deposits

RNA and DNA sequencing data as well as reconstructed Y/W sequences have been deposited in the Gene Expression Omnibus (GEO), Sequence Read Archive (SRA) and Transcriptome Shotgun Assembly (TSA) Database under the accession codes GSE50747, SRP029216, SRP026469 and PRJNA236159.

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Acknowledgements

We thank K. Harshman and the Lausanne Genomics Technology Facility for high-throughput sequencing support; I. Xenarios and the Vital-IT computational facility for computational support; S. Pääbo for great ape DNA samples; C. Roos for marmoset DNA samples; P. Jensen for chicken samples; E. Tsend-Ayush for help in determining the complete sequence of the AMHY gene in platypus; P. Gonzalez-Rubio for help with figure designs; M. Cardoso-Moreira, F. Carelli, A. Necsulea and M. Warnefors for comments on the manuscript; the Kaessmann group in general for discussions; and the Marmoset Genome Sequencing Consortium for making the marmoset genome assembly and annotation data available and for granting permission to use them for the analyses described in this study before publication. D.T.F. was supported by the Mexican National Council for Science and Technology (CONACyT). P.D.W. was supported by an ARC fellowship. F.G. was supported by an ARC fellowship. This research was supported by grants from the European Research Council (Starting Independent Grant: 242597, SexGenTransEvolution) and the Swiss National Science Foundation (Grant: 130287) to H.K.

Author information

Affiliations

  1. Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland

    • Diego Cortez
    • , Ray Marin
    • , Laure Froidevaux
    • , Angélica Liechti
    •  & Henrik Kaessmann
  2. Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland

    • Diego Cortez
    • , Ray Marin
    •  & Henrik Kaessmann
  3. The Robinson Research Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia

    • Deborah Toledo-Flores
    •  & Frank Grützner
  4. School of Biotechnology and Biomolecular Sciences, UNSW Australia, Sydney, New South Wales 2052, Australia

    • Paul D. Waters

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Contributions

D.C. performed most data processing and biological analyses. R.M. processed platypus genomic data and assessed X identity of contigs and the most likely chromosomal location of X gametologues in this species. D.T.-F. performed FISH experiments in platypus. L.F. and A.L. prepared samples and generated RNA-seq and genomic sequencing libraries. L.F. performed the large-scale PCR/Sanger sequencing validation experiments. P.D.W. provided elephant and tammar wallaby fibroblast samples and advised on these species’ sex chromosome biology. F.G. provided platypus and echidna samples, supervised FISH experiments, and provided advice on the sex chromosome biology of these species. The project was supervised and originally designed by H.K. The paper was written by D.C. and H.K. with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Diego Cortez or Henrik Kaessmann.

Extended data

Supplementary information

Zip files

  1. 1.

    Supplementary Dataset 1

    This zipped file contains all newly established Y and W sequences, CDS sequences of XY and ZW gametologs, the alignments of former pseudogenes in chimpanzee and relevant scripts. See the "SI Guide.txt" file in the folder for further details.

Excel files

  1. 1.

    Supplementary Tables 1-3

    Supplementary Tables 1-3 contain information regarding the RNA-seq and genomic data used in this study. The original file uploaded was corrupt and was replaced on 2 May 2014

  2. 2.

    Supplementary Table 4

    This Supplementary Table contains information regarding the Y transcript reconstruction pipeline. The original file uploaded was corrupt and was replaced on 2 May 2014

  3. 3.

    Supplementary Tables 5-18

    Supplementary Tables 5-18 contain information regarding Y and W genes in 13 mammals and chicken. The original file uploaded was corrupt and was replaced on 2 May 2014

  4. 4.

    Supplementary Tables 19-20

    Supplementary Tables 19 and 20 contain information regarding predicted X chromosome localization for X gametologs and statistical information about X-linked contigs in platypus. The original file uploaded was corrupt and was replaced on 2 May 2014

  5. 5.

    Supplementary Tables 21-23

    Supplementary Tables 21-23 contain information regarding GO terms enrichment among Y (W) genes and tissue-specificity analyses (statistics). The original file uploaded was corrupt and was replaced on 2 May 2014

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DOI

https://doi.org/10.1038/nature13151

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