The evolution of gene expression levels in mammalian organs

David Brawand; Magali Soumillon; Anamaria Necsulea; Philippe Julien; Gabor Csardi; Patrick Harrigan; Manuela Weier; Angelica Liechti; Ayinuer Aximu-Petri; Martin Kircher; Frank W. Albert; Ulrich Zeller; Philipp Khaitovich; Frank Gruetzner; Sven Bergmann; Rasmus Nielsen; Svante Paeaebo; Henrik Kaessmann

doi:10.1038/nature10532

The evolution of gene expression levels in mammalian organs

David Brawand, Magali Soumillon, Anamaria Necsulea, Philippe Julien, Gabor Csardi, Patrick Harrigan, Manuela Weier, Angelica Liechti, Ayinuer Aximu-Petri, Martin Kircher, Frank W. Albert, Ulrich Zeller, Philipp Khaitovich, Frank Gruetzner, Sven Bergmann, Rasmus Nielsen, Svante Paeaebo, Henrik Kaessmann

Computational and RNA Biology

665 Citations (Scopus)

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 language	English
Journal	Nature
Volume	478
Issue number	7369
Pages (from-to)	343-348
Number of pages	6
ISSN	0028-0836
DOIs	https://doi.org/10.1038/nature10532
Publication status	Published - 20 Oct 2011

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Brawand, D., Soumillon, M., Necsulea, A., Julien, P., Csardi, G., Harrigan, P., Weier, M., Liechti, A., Aximu-Petri, A., Kircher, M., Albert, F. W., Zeller, U., Khaitovich, P., Gruetzner, F., Bergmann, S., Nielsen, R., Paeaebo, S., & Kaessmann, H. (2011). The evolution of gene expression levels in mammalian organs. Nature, 478(7369), 343-348. https://doi.org/10.1038/nature10532

Brawand, D, Soumillon, M, Necsulea, A, Julien, P, Csardi, G, Harrigan, P, Weier, M, Liechti, A, Aximu-Petri, A, Kircher, M, Albert, FW, Zeller, U, Khaitovich, P, Gruetzner, F, Bergmann, S, Nielsen, R, Paeaebo, S & Kaessmann, H 2011, 'The evolution of gene expression levels in mammalian organs', Nature, vol. 478, no. 7369, pp. 343-348. https://doi.org/10.1038/nature10532

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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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AU - Harrigan, Patrick

AU - Weier, Manuela

AU - Liechti, Angelica

AU - Aximu-Petri, Ayinuer

AU - Kircher, Martin

AU - Albert, Frank W.

AU - Zeller, Ulrich

AU - Khaitovich, Philipp

AU - Gruetzner, Frank

AU - Bergmann, Sven

AU - Nielsen, Rasmus

AU - Paeaebo, Svante

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AB - 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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