The evolution of genetic networks by non-adaptive processes

Although numerous investigators assume that the global features of genetic networks are moulded by natural selection, there has been no formal demonstration of the adaptive origin of any genetic network. This Analysis shows that many of the qualitative features of known transcriptional networks can arise readily through the non-adaptive processes of genetic drift, mutation and recombination, raising questions about whether natural selection is necessary or even sufficient for the origin of many aspects of gene-network topologies. The widespread reliance on computational procedures that are devoid of population-genetic details to generate hypotheses for the evolution of network configurations seems to be unjustified.

[1]  M. Kimura,et al.  An introduction to population genetics theory , 1971 .

[2]  A. Clark,et al.  Invasion and maintenance of a gene duplication. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  R. Sommer Evolution and development — the nematode vulva as a case study , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

[4]  J. Gerhart,et al.  Cells, Embryos and Evolution , 1997 .

[5]  Araceli M. Huerta,et al.  From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. , 1998, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  E. Davidson,et al.  Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene. , 1998, Science.

[7]  A. Wagner,et al.  The role of population size, pleiotropy and fitness effects of mutations in the evolution of overlapping gene functions. , 2000, Genetics.

[8]  N. Johnson,et al.  Rapid speciation via parallel, directional selection on regulatory genetic pathways. , 2000, Journal of theoretical biology.

[9]  N. Patel,et al.  Evidence for stabilizing selection in a eukaryotic enhancer element , 2000, Nature.

[10]  R. Albert,et al.  The large-scale organization of metabolic networks , 2000, Nature.

[11]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[12]  R. R. Samaha,et al.  Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. , 2000, Science.

[13]  A. Wagner Robustness against mutations in genetic networks of yeast , 2000, Nature Genetics.

[14]  J. True,et al.  Developmental system drift and flexibility in evolutionary trajectories , 2001, Evolution & development.

[15]  A. Wilkins The Evolution of Developmental Pathways , 2001 .

[16]  J. Stone,et al.  Rapid evolution of cis-regulatory sequences via local point mutations. , 2001, Molecular biology and evolution.

[17]  A. Force,et al.  The probability of preservation of a newly arisen gene duplicate. , 2001, Genetics.

[18]  S. Shen-Orr,et al.  Network motifs in the transcriptional regulation network of Escherichia coli , 2002, Nature Genetics.

[19]  David J. Galas,et al.  A duplication growth model of gene expression networks , 2002, Bioinform..

[20]  Nicola J. Rinaldi,et al.  Transcriptional Regulatory Networks in Saccharomyces cerevisiae , 2002, Science.

[21]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[22]  Andreas Wagner,et al.  Convergent evolution of gene circuits , 2003, Nature Genetics.

[23]  Gary Ruvkun,et al.  Functional tests of enhancer conservation between distantly related species , 2003, Development.

[24]  Christos A Ouzounis,et al.  The phylogenetic diversity of eukaryotic transcription. , 2003, Nucleic acids research.

[25]  Gregory A. Wray,et al.  Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation , 2003, Development.

[26]  Fan Chung Graham,et al.  Duplication Models for Biological Networks , 2002, J. Comput. Biol..

[27]  Jason E Stajich,et al.  The effects of selection against spurious transcription factor binding sites. , 2003, Molecular biology and evolution.

[28]  Andreas Wagner,et al.  Does Selection Mold Molecular Networks? , 2003, Science's STKE.

[29]  U. Alon Biological Networks: The Tinkerer as an Engineer , 2003, Science.

[30]  E. Nimwegen Scaling Laws in the Functional Content of Genomes , 2003, physics/0307001.

[31]  R. Milo,et al.  Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Wuchty,et al.  Evolutionary cores of domain co-occurrence networks , 2005, BMC Evolutionary Biology.

[33]  Nicola J. Rinaldi,et al.  Transcriptional regulatory code of a eukaryotic genome , 2004, Nature.

[34]  David N. Messina,et al.  An ORFeome-based analysis of human transcription factor genes and the construction of a microarray to interrogate their expression. , 2004, Genome research.

[35]  M. Vergassola,et al.  An evolutionary and functional assessment of regulatory network motifs , 2005, Genome Biology.

[36]  Patrick C Phillips,et al.  The Opportunity for Canalization and the Evolution of Genetic Networks , 2004, The American Naturalist.

[37]  Sarel J Fleishman,et al.  Comment on "Network Motifs: Simple Building Blocks of Complex Networks" and "Superfamilies of Evolved and Designed Networks" , 2004, Science.

[38]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[39]  B. Snel,et al.  The yeast coexpression network has a small‐world, scale‐free architecture and can be explained by a simple model , 2004, EMBO reports.

[40]  Julio Collado-Vides,et al.  Phylogenetic distribution of DNA-binding transcription factors in bacteria and archaea , 2004, Comput. Biol. Chem..

[41]  Yury Goltsev,et al.  Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. , 2004, Developmental biology.

[42]  Evelyn Fox Keller,et al.  Revisiting "scale-free" networks. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[44]  James P Balhoff,et al.  Evolutionary analysis of the well characterized endo16 promoter reveals substantial variation within functional sites. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  COMPENSATORY EVOLUTION OF INTERACTING GENE PRODUCTS THROUGH MULTIFUNCTIONAL INTERMEDIATES , 2005, Evolution; international journal of organic evolution.

[46]  S. Carroll,et al.  Evolution at Two Levels: On Genes and Form , 2005, PLoS biology.

[47]  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.

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

[49]  Ricard V Solé,et al.  Topology, tinkering and evolution of the human transcription factor network , 2005, The FEBS journal.

[50]  Michael P H Stumpf,et al.  Complex networks and simple models in biology , 2005, Journal of The Royal Society Interface.

[51]  A. Wilkins Recasting developmental evolution in terms of genetic pathway and network evolution … and the implications for comparative biology , 2005, Brain Research Bulletin.

[52]  D V Foster,et al.  Network growth models and genetic regulatory networks. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  David A. Nix,et al.  Large-Scale Turnover of Functional Transcription Factor Binding Sites in Drosophila , 2006, PLoS Comput. Biol..

[54]  M Madan Babu,et al.  Uncovering a hidden distributed architecture behind scale-free transcriptional regulatory networks. , 2006, Journal of molecular biology.

[55]  D. Pilgrim,et al.  Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. , 2006, Developmental cell.

[56]  C. Wilke,et al.  Robustness and Evolvability in Living Systems , 2006 .

[57]  R. Solé,et al.  Are network motifs the spandrels of cellular complexity? , 2006, Trends in ecology & evolution.

[58]  C. Adami Digital genetics: unravelling the genetic basis of evolution , 2006, Nature Reviews Genetics.

[59]  E. Davidson,et al.  Gene Regulatory Networks and the Evolution of Animal Body Plans , 2006, Science.

[60]  J. Collado-Vides,et al.  Bacterial regulatory networks are extremely flexible in evolution , 2006, Nucleic acids research.

[61]  S. Teichmann,et al.  Evolutionary dynamics of prokaryotic transcriptional regulatory networks. , 2006, Journal of molecular biology.

[62]  D. Landsman,et al.  Multiple independent evolutionary solutions to core histone gene regulation , 2006, Genome Biology.

[63]  Otto X. Cordero,et al.  Feed-forward loop circuits as a side effect of genome evolution. , 2006, Molecular biology and evolution.

[64]  A. E. Tsong,et al.  Evolution of alternative transcriptional circuits with identical logic , 2006, Nature.

[65]  E. Davidson The Regulatory Genome: Gene Regulatory Networks In Development And Evolution , 2006 .

[66]  Sebastian Bonhoeffer,et al.  Evolution of complexity in signaling pathways , 2006, Proceedings of the National Academy of Sciences.

[67]  Andreas Wagner,et al.  Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology , 2007, PLoS Comput. Biol..

[68]  Andrew Meade,et al.  Assembly rules for protein networks derived from phylogenetic-statistical analysis of whole genomes , 2007, BMC Evolutionary Biology.

[69]  C. Ouzounis,et al.  Lineage-specific partitions in archaeal transcription. , 2007, Archaea.

[70]  J. Coyne,et al.  THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION , 2007, Evolution; international journal of organic evolution.

[71]  M. Lynch The frailty of adaptive hypotheses for the origins of organismal complexity , 2007, Proceedings of the National Academy of Sciences.