Abstract

Changes in gene expression are thought to underlie many of the phenotypic differences between species. However, large-scale analyses of gene expression evolution were until recently prevented by technological limitations. Here we report the sequencing of polyadenylated RNA from six organs across ten species that represent all major mammalian lineages (placentals, marsupials and monotremes) and birds (the evolutionary outgroup), with the goal of understanding the dynamics of mammalian transcriptome evolution. We show that the rate of gene expression evolution varies among organs, lineages and chromosomes, owing to differences in selective pressures: transcriptome change was slow in nervous tissues and rapid in testes, slower in rodents than in apes and monotremes, and rapid for the X chromosome right after its formation. Although gene expression evolution in mammals was strongly shaped by purifying selection, we identify numerous potentially selectively driven expression switches, which occurred at different rates across lineages and tissues and which probably contributed to the specific organ biology of various mammals.

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Accessions

Primary accessions

Gene Expression Omnibus

Data deposits

Sequencing data have been deposited in the Gene Expression Omnibus under accession code GSE30352.

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Acknowledgements

We thank K. Harshman and the LGTF for high-throughput sequencing support; I. Xenarios and the Vital-IT computational facility (Swiss Institute of Bioinformatics) for computational support; P. Jensen and L. Andersson for the red jungle fowl samples; E. Ait Yahya Graison and A. Reymond for C57BL/6J mouse RNA-seq data from male brain; C. Henrichsen and A. Reymond for wild-mouse samples; T. Daish, A. Casey, S. Lim, R. Jones and Glenrock station for platypus tissue collection and sample preparation; all other people and institutions that provided samples (Supplementary Table 1); W. Enard for ape sample organization; the members of the Kaessmann group for discussions; J. Meunier for statistical support; D. Cortez and M. Warnefors for comments on the manuscript; and R. Durbin and the Gorilla Genome Analysis Consortium for making the gorilla genome data available and for granting permission to use them for RNA-seq read mapping before publication. This research was supported by grants from the European Research Council (Starting Independent Researcher Grant: 242597, SexGenTransEvolution) and the Swiss National Science Foundation (grant 31003A_130287), to H.K. S.B. was supported by the Swiss National Science Foundation (grant 31003A_130691/1), the Swiss Institute of Bioinformatics and the European Framework Project 6 (AnEuploidy and EuroDia projects). S.P. was supported by the European Research Council (ERC-2008-AdG, TWOPAN) and by the Max Planck Society. A.N. was supported by a long-term FEBS postdoctoral fellowship. F.G. is an ARC Australian Research Fellow.

Author information

Author notes

    • Frank W. Albert

    Present address: Lewis Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA.

    • David Brawand
    • , Magali Soumillon
    •  & Anamaria Necsulea

    These authors contributed equally to this work.

Affiliations

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

    • David Brawand
    • , Magali Soumillon
    • , Anamaria Necsulea
    • , Philippe Julien
    • , Manuela Weier
    • , Angélica Liechti
    •  & Henrik Kaessmann
  2. Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland

    • David Brawand
    • , Magali Soumillon
    • , Anamaria Necsulea
    • , Philippe Julien
    • , Gábor Csárdi
    • , Sven Bergmann
    •  & Henrik Kaessmann
  3. Department of Medical Genetics, University of Lausanne, 1005 Lausanne, Switzerland

    • Gábor Csárdi
    •  & Sven Bergmann
  4. Department of Integrative Biology, University of California, Berkeley, California 94720, USA

    • Patrick Harrigan
    •  & Rasmus Nielsen
  5. Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany

    • Ayinuer Aximu-Petri
    • , Martin Kircher
    • , Frank W. Albert
    •  & Svante Pääbo
  6. Chair of Systematic Zoology, Humboldt-University, 10099 Berlin, Germany

    • Ulrich Zeller
  7. CAS-MPG Partner Institute for Computational Biology, 200031 Shanghai, China

    • Philipp Khaitovich
  8. The Robinson Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia

    • Frank Grützner
  9. The Bioinformatics Center, University of Copenhagen, 2200 Copenhagen, Denmark

    • Rasmus Nielsen

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Contributions

D.B., G.C., H.K., A.N. and P.H. performed biological data analyses. M.S. organized the RNA-seq data production. D.B. and A.N. processed and mapped the reads. A.N. refined genome annotations and established definitions and alignments of constitutive exons. M.S., A.L., F.W.A. and A.A.-P. prepared samples and generated RNA-seq libraries. M.W. prepared samples. P.J. contributed ideas regarding data analyses. F.W.A. coordinated ape RNA-seq data production. M.K. processed ape RNA-seq data. U.Z. extracted and organized Monodelphis domestica samples and advised on this species’ biology. P.K. organized Macaca mulatta samples and provided general advice on gene expression evolution. F.G. organized and extracted platypus RNA samples and advised on this species’ biology. P.H. developed the gene expression selection method and performed all corresponding analyses under the guidance of R.N. G.C. performed analyses using the iterative signature algorithm under the guidance of S.B. S.P. guided ape RNA-seq data production and processing. The project was supervised and originally designed by H.K. The paper was written by H.K. with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Henrik Kaessmann.

Supplementary information

PDF files

  1. 1.

    Supplementary Figures

    This file contains Supplementary Figures 1-9 with legends.

  2. 2.

    Supplementary Information

    This file contains Supplementary Notes, which include Supplementary Methods, Supplementary Results and a Supplementary Discussion; Supplementary Tables 1-12, Supplementary Figures 1-27 with legends and additional references.

Zip files

  1. 1.

    Supplementary Tables

    This zipped file contains 5 Supplementary Tables files as follows: Supplementary Tables 1-2 provide detailed information about all samples used in the study; Supplementary Table 3 provides examples of genes with sex-biased expression in various amniote species; Supplementary Tables 4-10 provide detailed data and overviews regarding transcription modules in the all-amniote and primate-specific datasets; Supplementary Tables 11-26 describe all statistically significant expression shifts of individual genes that occurred in the different amniote/primate lineages and Supplementary Tables 27-42 show the most overrepresented GO biological processes among lineage-specific expression changes of individual genes.

  2. 2.

    Supplementary Data 1

    This file provides all normalized expression values for all-amniote and primate-specific sets of orthologs.

  3. 3.

    Supplementary Data 2

    This file provides all normalized expression values for all-amniote and primate-specific sets of orthologs.

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DOI

https://doi.org/10.1038/nature10532

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