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

ELife
Karl R WottonJohannes Jaeger

Abstract

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.

References

Jan 24, 1992·Cell·D St Johnston, C Nüsslein-Volhard
Jan 1, 1987·Developmental Biology·J P PetschekA P Mahowald
Oct 30, 1980·Nature·C Nüsslein-Volhard, E Wieschaus
Jan 1, 1995·The Journal of Experimental Zoology·John ReinitzDavid H Sharp
Feb 11, 1993·Nature·J M SlackC F Graham
Feb 24, 1999·Molecular Biology and Evolution·J M HancockG A Dover
Mar 31, 1999·Proceedings of the National Academy of Sciences of the United States of America·Michael StauberUrs Schmidt-Ott
Feb 17, 2000·Nature·Michael Z LudwigMartin Kreitman
Jun 1, 2000·Theoretical Population Biology·Kenneth M Weiss, S M Fullerton
Sep 20, 2000·Proceedings of the National Academy of Sciences of the United States of America·Michael StauberUrs Schmidt-Ott
May 9, 2001·Evolution & Development·John True, Eric S Haag
Dec 1, 2001·Annual Review of Entomology·Gregory K Davis, Nipam H Patel
Jan 5, 2002·Proceedings of the National Academy of Sciences of the United States of America·Michael StauberUrs Schmidt-Ott
Jan 11, 2002·Developmental Biology·B StrunkD N Arnosti
Feb 15, 2002·Nature·Bahram HouchmandzadehStanislas Leibler
Jun 26, 2002·Molecular Biology and Evolution·Emmanouil T Dermitzakis, Andrew G Clark
Nov 16, 2002·Current Opinion in Genetics & Development·Michael Z Ludwig
Mar 18, 2004·Molecular and Cellular Endocrinology·Lawrence I Gilbert
Jul 16, 2004·Nature·Johannes JaegerJohn Reinitz
Jan 5, 2005·Nature Reviews. Genetics·Kenneth M Weiss
Mar 11, 2005·PLoS Biology·Michael Z LudwigMartin Kreitman
Mar 22, 2005·Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution·Einat Hazkani-CovoDan Graur
Nov 8, 2005·Current Biology : CB·Olivier Crauk, Nathalie Dostatni
May 20, 2006·PLoS Computational Biology·Theodore J PerkinsLeon Glass
Oct 17, 2006·PLoS Computational Biology·Alan M MosesMichael B Eisen
Feb 6, 2007·PLoS Computational Biology·S CilibertiAndreas Wagner
Aug 11, 2007·Proceedings of the National Academy of Sciences of the United States of America·S CilibertiAndreas Wagner
Dec 11, 2007·Developmental Biology·Svetlana SurkovaJohn Reinitz
Jan 4, 2008·Proceedings of the National Academy of Sciences of the United States of America·Ab Matteen RafiqiUrs Schmidt-Ott
Jan 25, 2008·Development Genes and Evolution·Michael StauberUrs Schmidt-Ott
May 27, 2008·Trends in Ecology & Evolution·Günter P Wagner, Vincent J Lynch
Jul 22, 2008·Evolution & Development·Steffen LemkeUrs Schmidt-Ott
Aug 30, 2008·Current Opinion in Genetics & Development·Carl-Philipp Heisenberg, Lilianna Solnica-Krezel
Mar 5, 2009·PloS One·Brant K PetersonMichael B Eisen
Oct 31, 2009·PLoS Computational Biology·Maksat AshyraliyevJohannes Jaeger
Jan 22, 2010·Nature·Jeremy A DraghiJoshua B Plotkin
May 1, 2010·Development·Steffen LemkeUrs Schmidt-Ott
May 4, 2010·Developmental Biology·Mónica A García-SolacheMichael Akam
Sep 14, 2010·Current Biology : CB·Mike Levine
Oct 12, 2010·Cellular and Molecular Life Sciences : CMLS·Johannes Jaeger
Dec 15, 2010·Nature·Alex T KalinkaPavel Tomancak
Dec 15, 2010·Nature·Tomislav Domazet-Lošo, Diethard Tautz
Mar 16, 2011·Proceedings of the National Academy of Sciences of the United States of America·Brian M WiegmannDavid K Yeates
Apr 5, 2011·Cold Spring Harbor Protocols·Ab Matteen RafiqiUrs Schmidt-Ott
Apr 5, 2011·Cold Spring Harbor Protocols·Ab Matteen RafiqiUrs Schmidt-Ott
Apr 5, 2011·Cold Spring Harbor Protocols·Ab Matteen RafiqiUrs Schmidt-Ott
Aug 30, 2011·Trends in Genetics : TIG·Andreas Wagner
Dec 7, 2011·Nature Reviews. Genetics·Patricia J Wittkopp, Gizem Kalay
Mar 6, 2012·Trends in Ecology & Evolution·Mihaela Pavlicev, Günter P Wagner
Mar 10, 2012·Science·Andres F SarrazinMichalis Averof
Jul 19, 2012·PLoS Computational Biology·Anton CrombachJohannes Jaeger
Aug 16, 2012·Molecular Systems Biology·Zeba WunderlichAngela H DePace
Sep 7, 2012·Nature·Marcel QuintIvo Grosse
Oct 30, 2012·Trends in Genetics : TIG·J Omar Yáñez-CunaAlexander Stark
Nov 15, 2012·Current Opinion in Genetics & Development·David L Richmond, Andrew C Oates
Feb 26, 2013·BMC Genomics·Eva Jiménez-GuriJohannes Jaeger
Nov 10, 2013·PLoS Computational Biology·Kolja BeckerJohannes Jaeger
Jan 11, 2014·PloS One·Karl R WottonJohannes Jaeger
Jan 11, 2014·PloS One·Eva Jiménez-GuriJohannes Jaeger
Jun 3, 2014·The Journal of Physiology·Johannes Jaeger, Nick Monk
Jan 1, 1986·Roux's Archives of Developmental Biology : the Official Organ of the EDBO·J Peter Gergen, E Wieschaus
Sep 1, 1984·Wilhelm Roux's Archives of Developmental Biology·Gerd JürgensH Kluding

Citations

Jan 23, 2016·Molecular Biology and Evolution·Anton CrombachJohannes Jaeger
Jul 12, 2016·Current Opinion in Genetics & Development·Urs Schmidt-Ott, Jeremy A Lynch
Nov 22, 2017·EvoDevo·Karl R WottonEva Jiménez-Guri
Apr 28, 2019·Genome Biology and Evolution·Marta Coronado-ZamoraIsaac Salazar-Ciudad
Jul 24, 2019·PLoS Computational Biology·Bhavin S Khatri, Richard A Goldstein
May 3, 2019·G3 : Genes - Genomes - Genetics·Zeba WunderlichAngela H DePace
Oct 18, 2019·G3 : Genes - Genomes - Genetics·Ben J VincentMark Rebeiz
Oct 19, 2019·G3 : Genes - Genomes - Genetics·David A FehrYen Lee Loh
Sep 19, 2018·Royal Society Open Science·Eva Jiménez-GuriJohannes Jaeger
Feb 6, 2017·PLoS Computational Biology·Berta VerdJohannes Jaeger
Jul 28, 2018·Genetics·Tobias UllerKevin N Laland

Methods Mentioned

BETA
gene knock-downs
PCR

Related Concepts

Metazoa
Diptera
Drosophila melanogaster
Embryonic Structures, Nonmammalian
Poly(A) Tail
Genes, Insect
Gene Expression Regulation, Developmental
Evolution, Molecular
Embryonic Pattern Formation
Drosophila melanogaster Proteins

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