The road to modularity

A network of interactions is called modular if it is subdivided into relatively autonomous, internally highly connected components. Modularity has emerged as a rallying point for research in developmental and evolutionary biology (and specifically evo–devo), as well as in molecular systems biology. Here we review the evidence for modularity and models about its origin. Although there is an emerging agreement that organisms have a modular organization, the main open problem is the question of whether modules arise through the action of natural selection or because of biased mutational mechanisms.

[1]  R. L. Berg,et al.  THE ECOLOGICAL SIGNIFICANCE OF CORRELATION PLEIADES , 1960 .

[2]  P. Grant Bill size, body size, and the ecological adaptations of bird species to competitive situations on islands. , 1968, Systematic zoology.

[3]  Rupert Riedl,et al.  Die Ordnung des Lebendigen : Systembedingungen der Evolution , 1975 .

[4]  W. Vent,et al.  Riedl, Rupert, Die Ordnung des Lebendigen. Systembedingungen der Evolution. 372 S., 317 Abb., 7 Tab. Verlag Paul Parey. Hamburg und Berlin, 1975 Preis: geb. DM 98,‐ , 1978 .

[5]  R. May,et al.  Stability and Complexity in Model Ecosystems , 1976, IEEE Transactions on Systems, Man, and Cybernetics.

[6]  R. Lande EFFECTIVE DEME SIZES DURING LONG‐TERM EVOLUTION ESTIMATED FROM RATES OF CHROMOSOMAL REARRANGEMENT , 1979, Evolution; international journal of organic evolution.

[7]  R. Lande QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY , 1979, Evolution; international journal of organic evolution.

[8]  P. Grant,et al.  Intense Natural Selection in a Population of Darwin's Finches (Geospizinae) in the Gal�pagos , 1981, Science.

[9]  P. Grant Inheritance of size and shape in a population of Darwin’s finches, Geospiza conirostris , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[11]  J. Fodor,et al.  The Modularity of Mind: An Essay on Faculty Psychology , 1984 .

[12]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[13]  S. Kosslyn,et al.  Why are What and Where Processed by Separate Cortical Visual Systems? A Computational Investigation , 1989, Journal of Cognitive Neuroscience.

[14]  W. Atchley,et al.  Development and Quantitative Genetics of Correlation Structure Among Body Parts of Drosophila melanogaster , 1990, The American Naturalist.

[15]  B. Grant,et al.  PHENOTYPIC AND GENETIC EFFECTS OF HYBRIDIZATION IN DARWIN'S FINCHES , 1994, Evolution; international journal of organic evolution.

[16]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[17]  J. Cheverud,et al.  Quantitative trait loci for murine growth. , 1996, Genetics.

[18]  G. Wagner HOMOLOGUES, NATURAL KINDS AND THE EVOLUTION OF MODULARITY , 1996 .

[19]  R. Raff Understanding Evolution: The Next Step. (Book Reviews: The Shape of Life. Genes, Development, and the Evolution of Animal Form.) , 1996 .

[20]  N. Wingreen,et al.  Emergence of Preferred Structures in a Simple Model of Protein Folding , 1996, Science.

[21]  J. Cheverud,et al.  PLEIOTROPIC EFFECTS OF INDIVIDUAL GENE LOCI ON MANDIBULAR MORPHOLOGY , 1997, Evolution; international journal of organic evolution.

[22]  N. Patel,et al.  Functional analysis of eve stripe 2 enhancer evolution in Drosophila: rules governing conservation and change. , 1998, Development.

[23]  J. Bonner Cells, embryos, and evolution: Toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability , 1998 .

[24]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Cheverud,et al.  Mapping quantitative trait loci for murine growth: a closer look at genetic architecture. , 1999, Genetical research.

[26]  P. Stadler,et al.  Viral RNA and evolved mutational robustness. , 1999, The Journal of experimental zoology.

[27]  Simon A. Levin,et al.  Fragile Dominion: Complexity and the Commons , 1999 .

[28]  C. Niehrs,et al.  Synexpression groups in eukaryotes , 1999, Nature.

[29]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[30]  J. Cheverud,et al.  Quantitative Trait Loci for Early‐ and Late‐Developing Skull Characters in Mice: A Test of the Genetic Independence Model of Morphological Integration , 1999, The American Naturalist.

[31]  H. Nemeschkal MORPHOMETRIC CORRELATION PATTERNS OF ADULT BIRDS (FRINGILLIDAE: PASSERIFORMES AND COLUMBIFORMES) MIRROR THE EXPRESSION OF DEVELOPMENTAL CONTROL GENES , 1999, Evolution; international journal of organic evolution.

[32]  J. Hopfield,et al.  From molecular to modular cell biology , 1999, Nature.

[33]  A. Leroi The scale independence of evolution , 2000, Evolution & development.

[34]  Patrik D'haeseleer,et al.  Genetic network inference: from co-expression clustering to reverse engineering , 2000, Bioinform..

[35]  G. P. Wagner,et al.  Is the genotype-phenotype map modular? A statistical approach using mouse quantitative trait loci data. , 2000, Genetics.

[36]  S. Carroll,et al.  Functional evolution of the Ultrabithorax protein. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D. Thieffry,et al.  Modularity in development and evolution. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[38]  James R. Knight,et al.  A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae , 2000, Nature.

[39]  W. Fontana,et al.  Plasticity, evolvability, and modularity in RNA. , 2000, The Journal of experimental zoology.

[40]  R. Winther Varieties of modules: kinds, levels, origins, and behaviors. , 2001, The Journal of experimental zoology.

[41]  A. Yang,et al.  Modularity, evolvability, and adaptive radiations: a comparison of the hemi‐ and holometabolous insects , 2001, Evolution & development.

[42]  P. Magwene NEW TOOLS FOR STUDYING INTEGRATION AND MODULARITY , 2001, Evolution; international journal of organic evolution.

[43]  G. Wagner The character concept in evolutionary biology , 2001 .

[44]  W. Fontana Modelling 'evo-devo' with RNA. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[45]  Gary D Bader,et al.  Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry , 2002, Nature.

[46]  Alessandro Vespignani,et al.  Immunization of complex networks. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  William McGinnis,et al.  Hox protein mutation and macroevolution of the insect body plan , 2002, Nature.

[48]  Yaniv Ziv,et al.  Revealing modular organization in the yeast transcriptional network , 2002, Nature Genetics.

[49]  P. Bork,et al.  Functional organization of the yeast proteome by systematic analysis of protein complexes , 2002, Nature.

[50]  N. Gostling,et al.  From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design , 2002, Heredity.

[51]  Ricard V. Solé,et al.  A Model of Large-Scale proteome Evolution , 2002, Adv. Complex Syst..

[52]  Roded Sharan,et al.  Discovering statistically significant biclusters in gene expression data , 2002, ISMB.

[53]  Marc S Halfon,et al.  Computation-based discovery of related transcriptional regulatory modules and motifs using an experimentally validated combinatorial model. , 2002, Genome research.

[54]  G. Stormo,et al.  Identification of a novel cis-regulatory element involved in the heat shock response in Caenorhabditis elegans using microarray gene expression and computational methods. , 2002, Genome research.

[55]  M. Laubichler Review of: Carroll, Sean B., Jennifer K. Grenier and Scott D. Weatherbee: From DNA to diversity : molecular genetics and the evolution of animal design. Malden, Mass [u.a.]: Blackwell Science 2001 , 2003 .

[56]  D. Pe’er,et al.  Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data , 2003, Nature Genetics.

[57]  Ricard V. Sole,et al.  Modularity "for free" in genome architecture? , 2003, q-bio/0312032.

[58]  Alexander Rives,et al.  Modular organization of cellular networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  T. F. Hansen Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. , 2003, Bio Systems.

[60]  J. Cheverud,et al.  Pleiotropic effects on mandibular morphology I. Developmental morphological integration and differential dominance. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[61]  G. P. Wagner,et al.  Examining the Modularity Concept in Evolutionary Psychology: The Level of Genes, Mind, and Culture , 2003 .

[62]  M. West-Eberhard Developmental plasticity and evolution , 2003 .

[63]  P. Brakefield,et al.  Concerted evolution and developmental integration in modular butterfly wing patterns , 2003, Evolution & development.

[64]  Berend Snel,et al.  Quantifying modularity in the evolution of biomolecular systems. , 2004, Genome research.

[65]  Lan V. Zhang,et al.  Evidence for dynamically organized modularity in the yeast protein–protein interaction network , 2004, Nature.

[66]  Jennifer Hallinan,et al.  Gene duplication and hierarchical modularity in intracellular interaction networks. , 2004, Bio Systems.

[67]  C. Amemiya,et al.  Comparative genomics, cis-regulatory elements, and gene duplication. , 2004, Methods in cell biology.

[68]  J. Cheverud,et al.  Pleiotropic effects on mandibular morphology II: differential epistasis and genetic variation in morphological integration. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[69]  R. Nielsen,et al.  Detecting Selection in Noncoding Regions of Nucleotide Sequences , 2004, Genetics.

[70]  Peter R. Grant,et al.  Bmp4 and Morphological Variation of Beaks in Darwin's Finches , 2004, Science.

[71]  B. Hallgrímsson,et al.  SERIAL HOMOLOGY AND THE EVOLUTION OF MAMMALIAN LIMB COVARIATION STRUCTURE , 2005, Evolution; international journal of organic evolution.

[72]  Lee Altenberg,et al.  Evolvability Suppression to Stabilize Far-Sighted Adaptations , 2005, Artificial Life.

[73]  A. Regev,et al.  Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Michael Lynch,et al.  The Origin of Subfunctions and Modular Gene Regulation , 2005, Genetics.

[75]  M. Lässig,et al.  Evolutionary population genetics of promoters: predicting binding sites and functional phylogenies. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[76]  U. Alon,et al.  Spontaneous evolution of modularity and network motifs. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[77]  J. Cheverud,et al.  Epistatic Pleiotropy and the Genetic Architecture of Covariation Within Early and Late-Developing Skull Trait Complexes in Mice , 2005, Genetics.

[78]  Hunter B. Fraser,et al.  Modularity and evolutionary constraint on proteins , 2005, Nature Genetics.

[79]  Günter P. Wagner,et al.  Complex Adaptations and the Evolution of Evolvability , 2005 .

[80]  P. Bork,et al.  Identification and analysis of evolutionarily cohesive functional modules in protein networks. , 2006, Genome research.

[81]  Hunter B. Fraser,et al.  Coevolution, modularity and human disease. , 2006, Current opinion in genetics & development.

[82]  A. Abzhanov,et al.  The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches , 2006, Nature.

[83]  J. Cheverud,et al.  The contribution of epistatic pleiotropy to the genetic architecture of covariation among polygenic traits in mice , 2006, Evolution & development.

[84]  B. Hall,et al.  Modularity and sense organs in the blind cavefish, Astyanax mexicanus , 2006, Evolution & development.

[85]  M. Tyers,et al.  Stratus Not Altocumulus: A New View of the Yeast Protein Interaction Network , 2006, PLoS biology.

[86]  C. Griswold,et al.  Pleiotropic mutation, modularity and evolvability , 2006, Evolution & development.

[87]  Nikolay V Dokholyan,et al.  The Coordinated Evolution of Yeast Proteins Is Constrained by Functional Modularity , 2022 .

[88]  C. Lovejoy,et al.  Growth plate formation and development in alligator and mouse metapodials: evolutionary and functional implications. , 2007, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[89]  Peter F Stadler,et al.  A stochastic model for the evolution of transcription factor binding site abundance. , 2007, Journal of theoretical biology.

[90]  M. Tyers,et al.  Still Stratus Not Altocumulus: Further Evidence against the Date/Party Hub Distinction , 2007, PLoS biology.

[91]  E. Ostrowski,et al.  A NEGATIVE RELATIONSHIP BETWEEN MUTATION PLEIOTROPY AND FITNESS EFFECT IN YEAST , 2007, Evolution; international journal of organic evolution.

[92]  Jianzhi Zhang,et al.  In Search of the Biological Significance of Modular Structures in Protein Networks , 2007, PLoS Comput. Biol..

[93]  T. F. Hansen,et al.  Comparing Variational Properties of Homologous Floral and Vegetative Characters in Dalechampia scandens: Testing the Berg Hypothesis , 2007, Evolutionary biology.

[94]  V. Latora,et al.  Detecting complex network modularity by dynamical clustering. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[95]  James M. Cheverud,et al.  GENETIC VARIATION IN PLEIOTROPY: DIFFERENTIAL EPISTASIS AS A SOURCE OF VARIATION IN THE ALLOMETRIC RELATIONSHIP BETWEEN LONG BONE LENGTHS AND BODY WEIGHT , 2007, Evolution; international journal of organic evolution.