Comparative transcriptome analyses reveal the evolution of gene expression levels in mammalian organs

David Brawand^1,2,11, Magali Soumillon^1,2,11, Anamaria Necsulea^1,2,11, Philippe Julien^1,2, Gábor Csárdi^2,3, Patrick Harrigan⁴, Manuela Weier¹, Angélica Liechti¹, Ayinuer Aximu-Petri⁵, Martin Kircher⁵, Frank W. Albert^5,6, Ulrich Zeller⁷, Philipp Khaitovich⁸, Frank Grützner⁹, Sven Bergmann^2,3, Rasmus Nielsen^4,10, Svante Pääbo⁵ & Henrik Kaessmann^1,2

• 1) Center for Integrative Genomics, University of Lausanne, Switzerland.
• 2) Swiss Institute of Bioinformatics.
• 3) Department of Medical Genetics, University of Lausanne, Lausanne, Switzerland.
• 4) Department of Integrative Biology, University of California, Berkeley, California, USA.
• 5) Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
• 6) Present address: Lewis Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USA.
• 7) Institute for Systematic Zoology, Humboldt-University, Berlin, Germany.
• 8) CAS-MPG Partner Institute for Computational Biology, Shanghai, PR China.
• 9) School of Molecular and Biomedical Science, University of Adelaide, Australia.
• 10) The Bioinformatics Center, University of Kopenhagen, Kopenhagen, Denmark.
• 11) These authors contributed equally to this work.

Abstract

Evolutionary changes in gene expression are thought to underlie many of the phenotypic differences between species. To understand the evolutionary dynamics of transcriptome change in mammals, we have sequenced polyadenylated RNA from six organs across ten species that represent all major mammalian lineages (placental mammals, marsupials, monotremes) as well as birds, the evolutionary outgroup. We use these data to refine current genome annotations and confirm that large proportions of mammalian genomes are transcribed. Gene expression phylogenies, which reflect remarkably well known species relationships, reveal that the rate of gene expression evolution varies among organs, lineages and chromosomes. For example, our analyses suggest that nervous tissues show slow and testes rapid transcriptome change due to differences in selective constraints; that regulatory evolution was slow in rodents due to increased efficiencies of purifying selection; and that the X chromosome experienced rapid adaptive expression evolution upon sex chromosome birth. Although gene expression evolution in mammals was strongly shaped by purifying selection, we identify numerous selectively driven expression switches, which occurred at different rates across lineages and tissues and apparently contributed to the specific organ biology of various mammals (e.g., of primate brains). Our transcriptome data provide a valuable resource for further functional and evolutionary analyses of mammalian genomes.

Citation

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. Comparative transcriptome analyses reveal the evolution of gene expression levels in mammalian organs