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PMID: 19139764 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Review

The evolution of hierarchical gene regulatory networks.

Nature reviews. Genetics ·Vol. 10 ·No. 2 ·2009-02-00 ·Pages 141-8

Erwin DH, Davidson EH

Abstract

Comparative developmental evidence indicates that reorganizations in developmental gene regulatory networks (GRNs) underlie evolutionary changes in animal morphology, including body plans. We argue here that the nature of the evolutionary alterations that arise from regulatory changes depends on the hierarchical position of the change within a GRN. This concept cannot be accomodated by microevolutionary nor macroevolutionary theory. It will soon be possible to investigate these ideas experimentally, by assessing the effects of GRN changes on morphological evolution.

MeSH Terms
Biological Evolution Gene Expression Regulation, Developmental Gene Regulatory Networks/genetics Models, Genetic Morphogenesis/genetics
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Erwin Douglas H
Department of Paleobiology, MRC-121, National Museum of Natural History, PO BOX 37012, Washington, Washington DC 20013-7012, USA. erwind@si.edu
Davidson Eric H
References (53)
53 references, click to expand
  1. Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4.
    Nature. 2006 May 11;441(7090):173-8 PMID: 16688168
  2. The evolutionary significance of cis-regulatory mutations.
    Nat Rev Genet. 2007 Mar;8(3):206-16 PMID: 17304246
  3. Phylogenetic footprinting analysis in the upstream regulatory regions of the Drosophila enhancer of split genes.
    Genetics. 2007 Nov;177(3):1377-94 PMID: 18039873
  4. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila.
    Nature. 2005 Feb 3;433(7025):481-7 PMID: 15690032
  5. Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution.
    Cell. 2006 Jun 30;125(7):1387-99 PMID: 16814723
  6. Collaboration between Smads and a Hox protein in target gene repression.
    Development. 2007 Oct;134(20):3585-92 PMID: 17855427
  7. The UBX-regulated network in the haltere imaginal disc of D. melanogaster.
    Dev Biol. 2007 Feb 15;302(2):717-27 PMID: 17174297
  8. Evolutionary developmental biology and the problem of variation.
    Evolution. 2000 Aug;54(4):1079-91 PMID: 11005278
  9. A view from the genome: spatial control of transcription in sea urchin development.
    Curr Opin Genet Dev. 1999 Oct;9(5):530-41 PMID: 10508696
  10. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism.
    Nature. 2003 Aug 21;424(6951):935-8 PMID: 12931187
  11. Gene regulatory networks and the evolution of animal body plans.
    Science. 2006 Feb 10;311(5762):796-800 PMID: 16469913
  12. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution.
    Cell. 2008 Jul 11;134(1):25-36 PMID: 18614008
  13. Expression of achaete-scute homologues in discrete proneural clusters on the developing notum of the medfly Ceratitis capitata, suggests a common origin for the stereotyped bristle patterns of higher Diptera.
    Development. 2000 Apr;127(7):1411-20 PMID: 10704387
  14. Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns.
    Development. 2002 Apr;129(8):1849-58 PMID: 11934851
  15. Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila.
    Development. 2005 Apr;132(7):1567-77 PMID: 15753212
  16. R11: a cis-regulatory node of the sea urchin embryo gene network that controls early expression of SpDelta in micromeres.
    Dev Biol. 2004 Oct 15;274(2):438-51 PMID: 15385170
  17. Regulatory divergence modifies limb length between mammals.
    Genes Dev. 2008 Jan 15;22(2):141-51 PMID: 18198333
  18. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks.
    Nature. 2004 Apr 15;428(6984):717-23 PMID: 15085123
  19. Parallel genetic origins of pelvic reduction in vertebrates.
    Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13753-8 PMID: 16945911
  20. The transcription/migration interface in heart precursors of Ciona intestinalis.
    Science. 2008 Jun 6;320(5881):1349-52 PMID: 18535245
  21. The evolution of transcriptional regulation in eukaryotes.
    Mol Biol Evol. 2003 Sep;20(9):1377-419 PMID: 12777501
  22. The evolution of gene regulation underlies a morphological difference between two Drosophila sister species.
    Cell. 2008 Mar 7;132(5):783-93 PMID: 18329365
  23. Mechanistic approaches to the study of evolution: the functional synthesis.
    Nat Rev Genet. 2007 Sep;8(9):675-88 PMID: 17703238
  24. cis-regulatory processing of Notch signaling input to the sea urchin glial cells missing gene during mesoderm specification.
    Dev Biol. 2006 Sep 15;297(2):587-602 PMID: 16925988
  25. Evolution of a transcriptional repression domain in an insect Hox protein.
    Nature. 2002 Feb 21;415(6874):910-3 PMID: 11859369
  26. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene.
    Nature. 2006 Apr 20;440(7087):1050-3 PMID: 16625197
  27. Experimentally based sea urchin gene regulatory network and the causal explanation of developmental phenomenology.
    Wiley Interdiscip Rev Syst Biol Med. 2009 Sep-Oct;1(2):237-246 PMID: 20228891
  28. The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches.
    Nature. 2006 Aug 3;442(7102):563-7 PMID: 16885984
  29. Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signaling.
    Genes Dev. 1994 Sep 1;8(17):2058-71 PMID: 7958878
  30. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution.
    Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6091-6 PMID: 18413604
  31. Molecular origins of rapid and continuous morphological evolution.
    Proc Natl Acad Sci U S A. 2004 Dec 28;101(52):18058-63 PMID: 15596718
  32. Shavenbaby couples patterning to epidermal cell shape control.
    PLoS Biol. 2006 Sep;4(9):e290 PMID: 16933974
  33. Insect appendages and comparative ontogenetics.
    Dev Biol. 2005 Oct 1;286(1):57-77 PMID: 16112665
  34. Dissecting early regulatory relationships in the lamprey neural crest gene network.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20083-8 PMID: 19104059
  35. A gene regulatory network armature for T lymphocyte specification.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20100-5 PMID: 19104054
  36. Of chicken wings and frog legs: a smorgasbord of evolutionary variation in mechanisms of tetrapod limb development.
    Dev Biol. 2005 Dec 1;288(1):21-39 PMID: 16246321
  37. The expression of pannier and achaete-scute homologues in a mosquito suggests an ancient role of pannier as a selector gene in the regulation of the dorsal body pattern.
    Development. 2002 Aug;129(16):3861-71 PMID: 12135924
  38. Molecular signaling in feather morphogenesis.
    Curr Opin Cell Biol. 2006 Dec;18(6):730-41 PMID: 17049829
  39. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13356-61 PMID: 14595011
  40. Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20089-94 PMID: 19104065
  41. Global regulatory logic for specification of an embryonic cell lineage.
    Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):5955-62 PMID: 18413610
  42. Hox protein mutation and macroevolution of the insect body plan.
    Nature. 2002 Feb 21;415(6874):914-7 PMID: 11859370
  43. Bmp4 and morphological variation of beaks in Darwin's finches.
    Science. 2004 Sep 3;305(5689):1462-5 PMID: 15353802
  44. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere.
    Genes Dev. 1998 May 15;12(10):1474-82 PMID: 9585507
  45. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution.
    Science. 1999 Jan 22;283(5401):532-4 PMID: 9915699
  46. Evo-Devo of amniote integuments and appendages.
    Int J Dev Biol. 2004;48(2-3):249-70 PMID: 15272390
  47. scute expression in Calliphora vicina reveals an ancestral pattern of longitudinal stripes on the thorax of higher Diptera.
    Development. 2002 Feb;129(3):563-72 PMID: 11830558
  48. How to pattern an epithelium: lessons from achaete-scute regulation on the notum of Drosophila.
    Gene. 2002 Jun 12;292(1-2):1-12 PMID: 12119094
  49. Morphological evolution through multiple cis-regulatory mutations at a single gene.
    Nature. 2007 Aug 2;448(7153):587-90 PMID: 17632547
  50. Evolution of yellow gene regulation and pigmentation in Drosophila.
    Curr Biol. 2002 Sep 17;12(18):1547-56 PMID: 12372246
  51. Genomic regulatory networks and animal development.
    Dev Cell. 2005 Oct;9(4):449-62 PMID: 16198288
  52. Caught in the evolutionary act: precise cis-regulatory basis of difference in the organization of gene networks of sea stars and sea urchins.
    Dev Biol. 2007 Dec 15;312(2):584-95 PMID: 17956756
  53. Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs.
    Genes Dev. 1995 Aug 1;9(15):1869-82 PMID: 7649474
Article Info
Journal
Nature reviews. Genetics
Abbr.
Nat Rev Genet
ISSN
1471-0064
DOI
10.1038/nrg2499
Email
erwind@si.edu
Published
2009-02-00
Epub
2009-00-13
Pages
141-8
Language
English
Region
England
NLM ID
100962779
Subset
IM
External Links
PubMed source DOI: 10.1038/nrg2499 View journal details
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