Regulation of gene expression is arguably the main mechanism underlying the phenotypic diversity of tissues within and between species. Here we assembled an extensive transcriptomic dataset covering 8 tissues across 20 bilaterian species and performed analyses using a symmetric phylogeny that allowed the combined and parallel investigation of gene expression evolution between vertebrates and insects. We specifically focused on widely conserved ancestral genes, identifying strong cores of pan-bilaterian tissue-specific genes and even larger groups that diverged to define vertebrate and insect tissues. Systematic inferences of tissue-specificity gains and losses show that nearly half of all ancestral genes have been recruited into tissue-specific transcriptomes. This occurred during both ancient and, especially, recent bilaterian evolution, with several gains being associated with the emergence of unique phenotypes (for example, novel cell types). Such pervasive evolution of tissue specificity was linked to gene duplication coupled with expression specialization of one of the copies, revealing an unappreciated prolonged effect of whole-genome duplications on recent vertebrate evolution.

Australian Regenerative Medicine Institute Monash University Clayton Victoria Australia

Biology and BSI Florida International University Miami FL USA

Centre for Ecology and Conservation University of Exeter Penryn UK

Centre for Genomic Regulation Barcelona Institute of Science and Technology Barcelona Spain

Department of Genetics Microbiology and Statistics and IRBio Universitat de Barcelona Barcelona Spain

Department of Parasitology University of South Bohemia České Budějovice Czech Republic

EMBL Australia; Victorian Node Monash University Clayton Victoria Australia

Eugene Bell Center for Regenerative Biology and Tissue Engineering Marine Biological Laboratory Woods Hole MA USA

ICREA Barcelona Spain

Institute of Evolutionary Biology Barcelona Catalonia Spain

Institute of Parasitology CAS České Budějovice Czech Republic

Sorbonne Université CNRS Biologie Intégrative des Organismes Marins; BIOM Banyuls sur Mer France

Stazione Zoologica Anton Dohrn Napoli Italy

Universitat Pompeu Fabra Barcelona Spain

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