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Pervasive evolution of tissue-specificity of ancestral genes differentially shaped vertebrates and insects

Federica Mantica, Luis P. Iñiguez, Yamile Marquez, Jon Permanyer, Antonio Torres-Mendez, Josefa Cruz, Xavi Franch-Marro, Frank Tulenko, Demian Burguera, View ORCID ProfileStephanie Bertrand, Toby Doyle, Marcela Nouzova, Peter Currie, Fernando G. Noriega, Hector Escriva, View ORCID ProfileMaria Ina Arnone, Caroline B Albertin, View ORCID ProfileKarl R Wotton, Isabel Almudi, David Martin, View ORCID ProfileManuel Irimia
doi: https://doi.org/10.1101/2022.11.14.516384
Federica Mantica
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Luis P. Iñiguez
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Yamile Marquez
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Jon Permanyer
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Antonio Torres-Mendez
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Josefa Cruz
2Institute of Evolutionary Biology (IBE, CSIC-Universitat Pompeu Fabra), Passeig de la Barceloneta 37, 08003 Barcelona, Catalonia, Spain
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Xavi Franch-Marro
2Institute of Evolutionary Biology (IBE, CSIC-Universitat Pompeu Fabra), Passeig de la Barceloneta 37, 08003 Barcelona, Catalonia, Spain
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Frank Tulenko
3Australian Regenerative Medicine Institute, Level 2, 15 Innovation Walk, Monash University, Wellington Road, Clayton, Victoria 3800, Australia
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Demian Burguera
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
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Stephanie Bertrand
4Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, F-66650, Banyuls-sur-Mer, France
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Toby Doyle
5Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, UK
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Marcela Nouzova
6Institute of Parasitology, CAS, České Budějovice, Czech Republic
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Peter Currie
3Australian Regenerative Medicine Institute, Level 2, 15 Innovation Walk, Monash University, Wellington Road, Clayton, Victoria 3800, Australia
7EMBL Australia, Victorian Node, Level 1, 15 Innovation Walk, Monash University, Wellington Road, Clayton, Victoria 3800, Australia
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Fernando G. Noriega
8Biology and BSI, Florida International University, Miami, USA
9Department of Parasitology, University of South Bohemia, České Budějovice, Czech Republic
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Hector Escriva
4Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, F-66650, Banyuls-sur-Mer, France
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Maria Ina Arnone
10Stazione Zoologica Anton Dohrn, villa comunale 80121, Napoli, Italy
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Caroline B Albertin
11Eugene Bell Center for Regenerative Biology and Tissue Engineering, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, USA
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Karl R Wotton
5Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn, UK
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Isabel Almudi
12Department of Genetics, Microbiology and Statistics and IRBio, Universitat de Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain
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David Martin
2Institute of Evolutionary Biology (IBE, CSIC-Universitat Pompeu Fabra), Passeig de la Barceloneta 37, 08003 Barcelona, Catalonia, Spain
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Manuel Irimia
1Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain
13Universitat Pompeu Fabra, Barcelona, Spain
14ICREA, Barcelona, Spain
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  • For correspondence: mirimia@gmail.com
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Abstract

Regulation of gene expression is arguably the main mechanism contributing to tissue phenotypic diversity within and between species. Here, we assembled a vast RNA-seq dataset covering twenty bilaterian species and eight tissues, selecting a specular phylogeny that allowed both 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-differential genes but even larger groups that diverged to define vertebrate and insect tissues. Consistently, 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 numerous gains being associated with the emergence of unique phenotypes. Such pervasive evolution of tissue-specificity was boosted by gene duplication coupled with specialization, including an unappreciated prolonged effect of whole genome duplications during recent vertebrate evolution.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted November 16, 2022.
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Pervasive evolution of tissue-specificity of ancestral genes differentially shaped vertebrates and insects
Federica Mantica, Luis P. Iñiguez, Yamile Marquez, Jon Permanyer, Antonio Torres-Mendez, Josefa Cruz, Xavi Franch-Marro, Frank Tulenko, Demian Burguera, Stephanie Bertrand, Toby Doyle, Marcela Nouzova, Peter Currie, Fernando G. Noriega, Hector Escriva, Maria Ina Arnone, Caroline B Albertin, Karl R Wotton, Isabel Almudi, David Martin, Manuel Irimia
bioRxiv 2022.11.14.516384; doi: https://doi.org/10.1101/2022.11.14.516384
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Pervasive evolution of tissue-specificity of ancestral genes differentially shaped vertebrates and insects
Federica Mantica, Luis P. Iñiguez, Yamile Marquez, Jon Permanyer, Antonio Torres-Mendez, Josefa Cruz, Xavi Franch-Marro, Frank Tulenko, Demian Burguera, Stephanie Bertrand, Toby Doyle, Marcela Nouzova, Peter Currie, Fernando G. Noriega, Hector Escriva, Maria Ina Arnone, Caroline B Albertin, Karl R Wotton, Isabel Almudi, David Martin, Manuel Irimia
bioRxiv 2022.11.14.516384; doi: https://doi.org/10.1101/2022.11.14.516384

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