The evolution of gene expression levels in mammalian organs

David Brawand, Magali Soumillon, Anamaria Necsulea, Philippe Julien, Gábor Csárdi, Patrick Harrigan, Manuela Weier, Angélica Liechti, Ayinuer Aximu-Petri, Martin Kircher, Frank W. Albert, Ulrich Zeller, Philipp Khaitovich, Frank Grützner, Sven Bergmann, Rasmus Nielsen, Svante Pääbo, Henrik Kaessmann

Research output: Contribution to journalArticlepeer-review

639 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)343-348
Number of pages6
JournalNature
Volume478
Issue number7369
DOIs
StatePublished - Oct 20 2011

Bibliographical note

Funding Information:
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 grantingpermissiontouse themfor RNA-seq readmappingbeforepublication.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.

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