Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria

Bilateria are the predominant clade of animals on Earth. Despite having evolved a wide variety of body plans and developmental modes, they are characterized by common morphological traits. By default, researchers have tried to link clade-specific genes to these traits, thus distinguishing bilaterian...

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Main Authors: Luca Ferretti, Andrea Krämer-Eis, Philipp H. Schiffer
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Life
Subjects:
Online Access:https://www.mdpi.com/2075-1729/10/9/182
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spelling doaj-6c81bba1b1b7459f95212f178d2799272020-11-25T03:06:47ZengMDPI AGLife2075-17292020-09-011018218210.3390/life10090182Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent BilateriaLuca Ferretti0Andrea Krämer-Eis1Philipp H. Schiffer2The Pirbright Institute, Ash Road, Pirbright, Surrey GU24 0NF, UKInstitut für Genetik, Universität zu Köln, Zülpicher Straße 47a, 50674 Köln, GermanyInstitut für Zoologie, Universität zu Köln, Zülpicher Straße 47b, 50674 Köln, GermanyBilateria are the predominant clade of animals on Earth. Despite having evolved a wide variety of body plans and developmental modes, they are characterized by common morphological traits. By default, researchers have tried to link clade-specific genes to these traits, thus distinguishing bilaterians from non-bilaterians, by their gene content. Here we argue that it is rather biological processes that unite Bilateria and set them apart from their non-bilaterian sisters, with a less complex body morphology. To test this hypothesis, we compared proteomes of bilaterian and non-bilaterian species in an elaborate computational pipeline, aiming to search for a set of bilaterian-specific genes. Despite the limited confidence in their bilaterian specificity, we nevertheless detected Bilateria-specific functional and developmental patterns in the sub-set of genes conserved in distantly related Bilateria. Using a novel multi-species GO-enrichment method, we determined the functional repertoire of genes that are widely conserved among Bilateria. Analyzing expression profiles in three very distantly related model species—<i>D. melanogaster</i>, <i>D. rerio</i> and <i>C. elegans</i>—we find characteristic peaks at comparable stages of development and a delayed onset of expression in embryos. In particular, the expression of the conserved genes appears to peak at the phylotypic stage of different bilaterian phyla. In summary, our study illustrate how development connects distantly related Bilateria after millions of years of divergence, pointing to processes potentially separating them from non-bilaterians. We argue that evolutionary biologists should return from a purely gene-centric view of evolution and place more focus on analyzing and defining conserved developmental processes and periods.https://www.mdpi.com/2075-1729/10/9/182evolutionbilateriagene ontologyexpression profiledevelopmentevodevo
collection DOAJ
language English
format Article
sources DOAJ
author Luca Ferretti
Andrea Krämer-Eis
Philipp H. Schiffer
spellingShingle Luca Ferretti
Andrea Krämer-Eis
Philipp H. Schiffer
Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
Life
evolution
bilateria
gene ontology
expression profile
development
evodevo
author_facet Luca Ferretti
Andrea Krämer-Eis
Philipp H. Schiffer
author_sort Luca Ferretti
title Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
title_short Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
title_full Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
title_fullStr Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
title_full_unstemmed Conserved Patterns in Developmental Processes and Phases, Rather than Genes, Unite the Highly Divergent Bilateria
title_sort conserved patterns in developmental processes and phases, rather than genes, unite the highly divergent bilateria
publisher MDPI AG
series Life
issn 2075-1729
publishDate 2020-09-01
description Bilateria are the predominant clade of animals on Earth. Despite having evolved a wide variety of body plans and developmental modes, they are characterized by common morphological traits. By default, researchers have tried to link clade-specific genes to these traits, thus distinguishing bilaterians from non-bilaterians, by their gene content. Here we argue that it is rather biological processes that unite Bilateria and set them apart from their non-bilaterian sisters, with a less complex body morphology. To test this hypothesis, we compared proteomes of bilaterian and non-bilaterian species in an elaborate computational pipeline, aiming to search for a set of bilaterian-specific genes. Despite the limited confidence in their bilaterian specificity, we nevertheless detected Bilateria-specific functional and developmental patterns in the sub-set of genes conserved in distantly related Bilateria. Using a novel multi-species GO-enrichment method, we determined the functional repertoire of genes that are widely conserved among Bilateria. Analyzing expression profiles in three very distantly related model species—<i>D. melanogaster</i>, <i>D. rerio</i> and <i>C. elegans</i>—we find characteristic peaks at comparable stages of development and a delayed onset of expression in embryos. In particular, the expression of the conserved genes appears to peak at the phylotypic stage of different bilaterian phyla. In summary, our study illustrate how development connects distantly related Bilateria after millions of years of divergence, pointing to processes potentially separating them from non-bilaterians. We argue that evolutionary biologists should return from a purely gene-centric view of evolution and place more focus on analyzing and defining conserved developmental processes and periods.
topic evolution
bilateria
gene ontology
expression profile
development
evodevo
url https://www.mdpi.com/2075-1729/10/9/182
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