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

David Brawand1,2,11, Magali Soumillon1,2,11, Anamaria Necsulea1,2,11, Philippe Julien1,2, Gábor Csárdi2,3, Patrick Harrigan4, Manuela Weier1, Angélica Liechti1, Ayinuer Aximu-Petri5, Martin Kircher5, Frank W. Albert5,6, Ulrich Zeller7, Philipp Khaitovich8, Frank Grützner9, Sven Bergmann2,3, Rasmus Nielsen4,10, Svante Pääbo5 & Henrik Kaessmann1,2


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.


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