Specialization Can Drive the Evolution of Modularity

Organismal development and many cell biological processes are organized in a modular fashion, where regulatory molecules form groups with many interactions within a group and few interactions between groups. Thus, the activity of elements within a module depends little on elements outside of it. Modularity facilitates the production of heritable variation and of evolutionary innovations. There is no consensus on how modularity might evolve, especially for modules in development. We show that modularity can increase in gene regulatory networks as a byproduct of specialization in gene activity. Such specialization occurs after gene regulatory networks are selected to produce new gene activity patterns that appear in a specific body structure or under a specific environmental condition. Modules that arise after specialization in gene activity comprise genes that show concerted changes in gene activities. This and other observations suggest that modularity evolves because it decreases interference between different groups of genes. Our work can explain the appearance and maintenance of modularity through a mechanism that is not contingent on environmental change. We also show how modularity can facilitate co-option, the utilization of existing gene activity to build new gene activity patterns, a frequent feature of evolutionary innovations.

[1]  C. Waddington,et al.  The strategy of the genes , 1957 .

[2]  C. Waddington.  The strategy of the genes , 1957 .

[3]  W. Barker.  Ontogeny and phylogeny. , 1980, Archives of surgery.

[4]  David H. Sharp,et al.  A connectionist model of development. , 1991, Journal of theoretical biology.

[5]  Kurt Mehlhorn,et al.  LEDA: a platform for combinatorial and geometric computing , 1997, CACM.

[6]  A. Wagner.  DOES EVOLUTIONARY PLASTICITY EVOLVE? , 1996, Evolution; international journal of organic evolution.

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

[8]  J. Fincham,et al.  At Home in the Universe: the Search for Laws of Complexity . By Stuart Kauffman. Viking 1995. viii + 321 pages. Hard cover. Price £20. ISBN 0 670 84735 6. , 1996 .

[9]  S. Carroll,et al.  Fossils, genes and the evolution of animal limbs , 1997, Nature.

[10]  M. Cohn,et al.  Hox9 genes and vertebrate limb specification , 1997, nature.

[11]  E. Álvarez-Buylla,et al.  Dynamics of the genetic regulatory network for Arabidopsis thaliana flower morphogenesis. , 1998, Journal of theoretical biology.

[12]  D. Weigel,et al.  A genetic framework for floral patterning , 1998, Nature.

[13]  G. von Dassow,et al.  Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. , 1999, The Journal of experimental zoology.

[14]  Bret J. Pearson,et al.  Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. , 1999, Science.

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

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

[17]  Jessica A. Bolker,et al.  Modularity in Development and Why It Matters to Evo-Devo1 , 2000 .

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

[19]  G. Odell,et al.  The segment polarity network is a robust developmental module , 2000, Nature.

[20]  D. Botstein,et al.  Genomic expression programs in the response of yeast cells to environmental changes. , 2000, Molecular biology of the cell.

[21]  M. Lenhard,et al.  Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS , 2001, Cell.

[22]  E. Lander,et al.  Remodeling of yeast genome expression in response to environmental changes. , 2001, Molecular biology of the cell.

[23]  T. Williams,et al.  Developmental modularity and the evolutionary diversification of arthropod limbs. , 2001, The Journal of experimental zoology.

[24]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[25]  A. Bergman,et al.  Waddington's canalization revisited: Developmental stability and evolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Odell,et al.  Design and constraints of the Drosophila segment polarity module: robust spatial patterning emerges from intertwined cell state switches. , 2002, The Journal of experimental zoology.

[27]  G. Odell,et al.  Robustness, Flexibility, and the Role of Lateral Inhibition in the Neurogenic Network , 2002, Current Biology.

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

[29]  L. Hood,et al.  A Genomic Regulatory Network for Development , 2002, Science.

[30]  G. K. Davis,et al.  Short, long, and beyond: molecular and embryological approaches to insect segmentation. , 2002, Annual review of entomology.

[31]  G. Wagner,et al.  EVOLUTION AND DETECTION OF GENETIC ROBUSTNESS , 2003 .

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

[33]  J. Pronk,et al.  The Genome-wide Transcriptional Responses of Saccharomyces cerevisiae Grown on Glucose in Aerobic Chemostat Cultures Limited for Carbon, Nitrogen, Phosphorus, or Sulfur* , 2003, The Journal of Biological Chemistry.

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

[35]  R. Guimerà,et al.  Modularity from fluctuations in random graphs and complex networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[36]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[37]  Nicholas T Ingolia,et al.  Topology and Robustness in the Drosophila Segment Polarity Network , 2004, PLoS biology.

[38]  A. Wagner.  Robustness and Evolvability in Living Systems , 2005 .

[39]  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.

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

[41]  Gabriel S. Eichler,et al.  Cell fates as high-dimensional attractor states of a complex gene regulatory network. , 2005, Physical review letters.

[42]  R. Guimerà,et al.  Functional cartography of complex metabolic networks , 2005, Nature.

[43]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[44]  M E J Newman,et al.  Modularity and community structure in networks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Feder.  Robustness and Evolvability in Living Systems. Princeton Studies in Complexity.By Andreas Wagner. Princeton (New Jersey): Princeton University Press. $49.50. xv + 367 p; ill.; index. ISBN: 0–691–12240–7. 2005. , 2006 .

[46]  Todd H. Oakley,et al.  Repression and loss of gene expression outpaces activation and gain in recently duplicated fly genes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Kristen K. Dang,et al.  Sexual reproduction selects for robustness and negative epistasis in artificial gene networks , 2006, Nature.

[48]  G. Wagner,et al.  The road to modularity , 2007, Nature Reviews Genetics.

[49]  A. Wagner.  Robustness and evolvability: a paradox resolved , 2008, Proceedings of the Royal Society B: Biological Sciences.

[50]  S. Fortunato,et al.  Resolution limit in community detection , 2006, Proceedings of the National Academy of Sciences.

[51]  A. Wagner,et al.  Innovation and robustness in complex regulatory gene networks , 2007, Proceedings of the National Academy of Sciences.

[52]  U. Alon,et al.  Environmental variability and modularity of bacterial metabolic networks , 2007, BMC Evolutionary Biology.

[53]  B. Spiegelman,et al.  PRDM16 controls a brown fat/skeletal muscle switch , 2008, Nature.

[54]  D. Arendt.  The evolution of cell types in animals: emerging principles from molecular studies , 2008, Nature Reviews Genetics.

[55]  E. Davidson,et al.  Global regulatory logic for specification of an embryonic cell lineage , 2008, Proceedings of the National Academy of Sciences.

[56]  Arend Hintze,et al.  Evolution of Complex Modular Biological Networks , 2007, PLoS Comput. Biol..

[57]  Robert D. Leclerc.  Survival of the sparsest: robust gene networks are parsimonious , 2008, Molecular systems biology.

[58]  A. Wagner,et al.  Multifunctionality and robustness trade-offs in model genetic circuits. , 2008, Biophysical journal.

[59]  E. Davidson,et al.  Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution , 2008, Proceedings of the National Academy of Sciences.

[60]  E. Stone,et al.  Systems Genetics of Complex Traits in Drosophila melanogaster , 2009, Nature Genetics.

[61]  G. Fraser,et al.  An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws , 2009, PLoS biology.

[62]  G. Wagner,et al.  The evolutionary dynamics of evolvability in a gene network model , 2009, Journal of evolutionary biology.

[63]  S. Carroll,et al.  Deep homology and the origins of evolutionary novelty , 2009, Nature.