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The hourglass model of evolutionary conservation during embryogenesis extends to developmental enhancers with signatures of positive selection

View ORCID ProfileJialin Liu, Rebecca R. Viales, View ORCID ProfilePierre Khoueiry, View ORCID ProfileJames P. Reddington, View ORCID ProfileCharles Girardot, View ORCID ProfileEileen E. M. Furlong, View ORCID ProfileMarc Robinson-Rechavi
doi: https://doi.org/10.1101/2020.11.02.364505
Jialin Liu
1Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
2Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
4Biozentrum, University of Basel, Basel, Switzerland
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Rebecca R. Viales
3European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany
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Pierre Khoueiry
3European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany
5American University of Beirut (AUB), Department of Biochemistry and Molecular Genetics, Beirut, Lebanon
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James P. Reddington
3European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany
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Charles Girardot
3European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany
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Eileen E. M. Furlong
3European Molecular Biology Laboratory, Genome Biology Unit, Heidelberg, Germany
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  • For correspondence: eileen.furlong@embl.org marc.robinson-rechavi@unil.ch
Marc Robinson-Rechavi
1Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
2Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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  • For correspondence: eileen.furlong@embl.org marc.robinson-rechavi@unil.ch
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Abstract

Inter-species comparisons of both morphology and gene expression within a phylum have revealed a period in the middle of embryogenesis with more similarity between species compared to earlier and later time-points. This ‘developmental hourglass’ pattern has been observed in many phyla, yet the evolutionary constraints on gene expression, and underlying mechanisms of how this is regulated, remains elusive. Moreover, the role of positive selection on gene regulation in the more diverged earlier and later stages of embryogenesis remains unknown. Here, using DNase-seq to identify regulatory regions in two distant Drosophila species (D. melanogaster and D. virilis), we assessed the evolutionary conservation and adaptive evolution of enhancers throughout multiple stages of embryogenesis. This revealed a higher proportion of conserved enhancers at the phylotypic period, providing a regulatory basis for the hourglass expression pattern. Using an in silico mutagenesis approach, we detect signatures of positive selection on developmental enhancers at early and late stages of embryogenesis, with a depletion at the phylotypic period, suggesting positive selection as one evolutionary mechanism underlying the hourglass pattern of animal evolution.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/ljljolinq1010/Chromatin-accessibility-evolution-during-Drosophilaembryogenesis

Copyright 
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 4.0 International license.
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Posted November 02, 2020.
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The hourglass model of evolutionary conservation during embryogenesis extends to developmental enhancers with signatures of positive selection
Jialin Liu, Rebecca R. Viales, Pierre Khoueiry, James P. Reddington, Charles Girardot, Eileen E. M. Furlong, Marc Robinson-Rechavi
bioRxiv 2020.11.02.364505; doi: https://doi.org/10.1101/2020.11.02.364505
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The hourglass model of evolutionary conservation during embryogenesis extends to developmental enhancers with signatures of positive selection
Jialin Liu, Rebecca R. Viales, Pierre Khoueiry, James P. Reddington, Charles Girardot, Eileen E. M. Furlong, Marc Robinson-Rechavi
bioRxiv 2020.11.02.364505; doi: https://doi.org/10.1101/2020.11.02.364505

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