Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita

The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (...

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Main Authors: Karl R Wotton, Eva Jiménez-Guri, Anton Crombach, Hilde Janssens, Anna Alcaine-Colet, Steffen Lemke, Urs Schmidt-Ott, Johannes Jaeger
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/04785
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author Karl R Wotton
Eva Jiménez-Guri
Anton Crombach
Hilde Janssens
Anna Alcaine-Colet
Steffen Lemke
Urs Schmidt-Ott
Johannes Jaeger
author_facet Karl R Wotton
Eva Jiménez-Guri
Anton Crombach
Hilde Janssens
Anna Alcaine-Colet
Steffen Lemke
Urs Schmidt-Ott
Johannes Jaeger
author_sort Karl R Wotton
collection DOAJ
description The segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution.
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spelling doaj.art-2070acfada30441ab4cc352781a9eac72022-12-22T03:52:37ZengeLife Sciences Publications LtdeLife2050-084X2015-01-01410.7554/eLife.04785Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abditaKarl R Wotton0https://orcid.org/0000-0002-8672-9948Eva Jiménez-Guri1https://orcid.org/0000-0002-9592-1077Anton Crombach2Hilde Janssens3Anna Alcaine-Colet4Steffen Lemke5Urs Schmidt-Ott6Johannes Jaeger7https://orcid.org/0000-0002-2568-2103European Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, SpainEuropean Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, SpainEuropean Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, SpainEuropean Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, SpainEuropean Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, Spain; Universitat de Barcelona, Barcelona, SpainDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, United StatesDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, United StatesEuropean Molecular Biology Laboratory, CRG Systems Biology Research Unit, Centre for Genomic Regulation, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, SpainThe segmentation gene network in insects can produce equivalent phenotypic outputs despite differences in upstream regulatory inputs between species. We investigate the mechanistic basis of this phenomenon through a systems-level analysis of the gap gene network in the scuttle fly Megaselia abdita (Phoridae). It combines quantification of gene expression at high spatio-temporal resolution with systematic knock-downs by RNA interference (RNAi). Initiation and dynamics of gap gene expression differ markedly between M. abdita and Drosophila melanogaster, while the output of the system converges to equivalent patterns at the end of the blastoderm stage. Although the qualitative structure of the gap gene network is conserved, there are differences in the strength of regulatory interactions between species. We term such network rewiring ‘quantitative system drift’. It provides a mechanistic explanation for the developmental hourglass model in the dipteran lineage. Quantitative system drift is likely to be a widespread mechanism for developmental evolution.https://elifesciences.org/articles/04785evolutionary developmental biologydevelopmental system driftgap gene networkRNA interferencedata quantificationMegaselia abdita
spellingShingle Karl R Wotton
Eva Jiménez-Guri
Anton Crombach
Hilde Janssens
Anna Alcaine-Colet
Steffen Lemke
Urs Schmidt-Ott
Johannes Jaeger
Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
eLife
evolutionary developmental biology
developmental system drift
gap gene network
RNA interference
data quantification
Megaselia abdita
title Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
title_full Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
title_fullStr Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
title_full_unstemmed Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
title_short Quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly Megaselia abdita
title_sort quantitative system drift compensates for altered maternal inputs to the gap gene network of the scuttle fly megaselia abdita
topic evolutionary developmental biology
developmental system drift
gap gene network
RNA interference
data quantification
Megaselia abdita
url https://elifesciences.org/articles/04785
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