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Toward a Theory of Multilevel Evolution: Long-Term Information Integration Shapes the Mutational Landscape and Enhances Evolvability

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Part of the book series: Advances in Experimental Medicine and Biology ((volume 751))

Abstract

Most of evolutionary theory has abstracted away from how information is coded in the genome and how this information is transformed into traits on which selection takes place. While in the earliest stages of biological evolution, in the RNA world, the mapping from the genotype into function was largely predefined by the physical–chemical properties of the evolving entities (RNA replicators, e.g. from sequence to folded structure and catalytic sites), in present-day organisms, the mapping itself is the result of evolution. I will review results of several in silico evolutionary studies which examine the consequences of evolving the genetic coding, and the ways this information is transformed, while adapting to prevailing environments. Such multilevel evolution leads to long-term information integration. Through genome, network, and dynamical structuring, the occurrence and/or effect of random mutations becomes nonrandom, and facilitates rapid adaptation. This is what does happen in the in silico experiments. Is it also what did happen in biological evolution? I will discuss some data that suggest that it did. In any case, these results provide us with novel search images to tackle the wealth of biological data.

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Notes

  1. 1.

    This dictum is often attributed to Einstein (e.g., [42]), although he has never said it in this form. Nevertheless, it remains a nice pointer to emphasize that on the one hand, models should not incorporate unnecessary detail, but on the other hand should not overlook (and therewith obscure) essential features of the process modeled.

  2. 2.

    DNA can, in fact, be a catalyst as well, but in the model, we define it as noncatalytic as it is in present-day systems.

  3. 3.

    In this model, we do not distinguish + strands and − strands.

References

  1. Adami C, Ofria C, Collier TC (2000) Evolution of biological complexity. Proc Natl Acad Sci 97(9):4463

    Article  PubMed  CAS  Google Scholar 

  2. Barabási AL, Albert R (1999) Emergence of scaling in random networks. Science 286(5439):509

    Article  PubMed  Google Scholar 

  3. Boerlijst M, Hogeweg P (1992) Self-structuring and selection: Spiral waves as a substrate for prebiotic evolution. In: In: Langton CG, Taylor C, Farmer JD, Rasmussen S (eds) Artificial Life II pp. 255–276

    Google Scholar 

  4. Boerlijst MC, Hogeweg P (1991) Spiral wave structure in pre-biotic evolution: Hypercycles stable against parasites. Phys D Nonlin Phenom 48(1):17–28

    Article  Google Scholar 

  5. Ciliberti S, Martin OC, Wagner A (2007) Innovation and robustness in complex regulatory gene networks. Proc Natl Acad Sci 104(34):13591

    Article  PubMed  CAS  Google Scholar 

  6. Cordero OX, Hogeweg P (2006) Feed-forward loop circuits as a side effect of genome evolution. Mol Biol Evol 23(10):1931

    Article  PubMed  CAS  Google Scholar 

  7. Crick F (1971) Central dogma of molecular biology. Tsitologiia 13(7):906

    CAS  Google Scholar 

  8. Crombach A, Hogeweg P (2007) Chromosome rearrangements and the evolution of genome structuring and adaptability. Mol Biol Evol 24(5):1130

    Article  PubMed  CAS  Google Scholar 

  9. Crombach A, Hogeweg P (2008) Evolution of evolvability in gene regulatory networks. PLoS Comput Biol 4(7):e1000112

    Article  PubMed  Google Scholar 

  10. Cuypers TD, Hogeweg P (2012) Virtual genomes in flux: An interplay of neutrality and adaptability explains genome expansion and streamlining. Genome Biol Evol 4(3):212–229

    Article  PubMed  CAS  Google Scholar 

  11. David LA, Alm EJ (2011) Rapid evolutionary innovation during an archaean genetic expansion. Nature 480(7376):241–244

    Article  PubMed  Google Scholar 

  12. de Boer F, Hogeweg P (2010) Eco-evolutionary dynamics, coding structure and the information threshold. BMC Evol Biol 10(1):361

    Article  PubMed  Google Scholar 

  13. Draghi J, Wagner GP (2009) The evolutionary dynamics of evolvability in a gene network model. J Evol Biol 22(3):599–611

    Article  PubMed  CAS  Google Scholar 

  14. Draghi JA, Parsons TL, Wagner GP, Plotkin JB (2010) Mutational robustness can facilitate adaptation. Nature 463(7279):353–355

    Article  PubMed  CAS  Google Scholar 

  15. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, Botstein D (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci 99(25):16144

    Article  PubMed  CAS  Google Scholar 

  16. Ferea TL, Botstein D, Brown PO, Rosenzweig RF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci 96(17):9721

    Article  PubMed  CAS  Google Scholar 

  17. Ferrada E, Wagner A (2008) Protein robustness promotes evolutionary innovations on large evolutionary time-scales. Proc Roy Soc B Biol Sci 275(1643):1595

    Article  CAS  Google Scholar 

  18. Fontana W (2002) Modelling  evo-devo with RNA. BioEssays 24(12):1164–1177

    Article  PubMed  CAS  Google Scholar 

  19. Fontana W, Schuster P (1998) Continuity in evolution: on the nature of transitions. Science 280(5368):1451

    Article  PubMed  CAS  Google Scholar 

  20. Fontana W, Stadler PF, Bornberg-Bauer EG, Griesmacher T, Hofacker IL, Tacker M, Tarazona P, Weinberger ED, Schuster P (1993) RNA folding and combinatory landscapes. Phys Rev E 47(3):2083–2099

    Article  CAS  Google Scholar 

  21. Francino MP (2005) An adaptive radiation model for the origin of new gene functions. Nat Genet 37(6):573

    Article  PubMed  CAS  Google Scholar 

  22. Grüner W, Giegerich R, Strothmann D, Reidys C, Weber J, Hofacker IL, Stadler PF, Schuster P (1996) Analysis of rna sequence structure maps by exhaustive enumeration I. Neutral networks. Monatsh Chem Chem Mon 127(4):355–374

    Google Scholar 

  23. Hahn MW, Han MV, Han SG (2007) Gene family evolution across 12 drosophila genomes. PLoS Genet 3(11):e197

    Article  PubMed  Google Scholar 

  24. Hogeweg P (2011) The roots of bioinformatics in theoretical biology. PLoS Comput Biol 7(3):e1002021

    Article  PubMed  CAS  Google Scholar 

  25. Hogeweg P, Hesper B (1984) Energy directed folding of rna sequences. Nucleic Acids Res 12(1 Pt 1):67

    Article  PubMed  CAS  Google Scholar 

  26. Hogeweg P, Hesper B (1989) An adaptive, selfmodifying, non goal directed modelling methodology. In: Elzas MS, Oren TI, Zeigler BP (eds) Knowledge systems paradigms. Elsevier Science, North Holland, pp 77–92

    Google Scholar 

  27. Hogeweg P, Takeuchi N (2003) Multilevel selection in models of prebiotic evolution: compartments and spatial self-organization. Orig Life Evol Biosph 33(4):375–403

    Article  PubMed  CAS  Google Scholar 

  28. Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez È, Blow MJ, Bronner-Fraser M, Brunet F, Butts T, Candiani S, Dishaw LJ et al (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18(7):1100

    Article  PubMed  CAS  Google Scholar 

  29. Hurst LD, Pál C, Lercher MJ (2004) The evolutionary dynamics of eukaryotic gene order. Nat Rev Genet 5(4):299–310

    Article  PubMed  CAS  Google Scholar 

  30. Huynen MA (1996) Exploring phenotype space through neutral evolution. J Mol Evol 43(3):165–169

    Article  PubMed  CAS  Google Scholar 

  31. Huynen MA, Hogeweg P (1994) Pattern generation in molecular evolution: Exploitation of the variation in RNA landscapes. J Mol Evol 39(1):71–79

    Article  PubMed  Google Scholar 

  32. Huynen MA, Stadler PF, Fontana W (1996) Smoothness within ruggedness: The role of neutrality in adaptation. Proc Natl Acad Sci USA 93(1):397

    Article  PubMed  CAS  Google Scholar 

  33. Huynen MA, Snel B, Bork P, Gibson TJ (2001) The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum Mol Genet 10(21):2463

    Article  PubMed  CAS  Google Scholar 

  34. Kacser H, Beeby R (1984) Evolution of catalytic proteins. J Mol Evol 20(1):38–51

    Article  PubMed  CAS  Google Scholar 

  35. Kashtan N, Itzkovitz S, Milo R, Alon U (2004) Topological generalizations of network motifs. Phys Rev E 70(3):031909

    Article  CAS  Google Scholar 

  36. Kauffman S, Levin S (1987) Toward a general theory of adaptive walks on rugged landscapes*. J Theor Biol 128(1):11–45

    Article  PubMed  CAS  Google Scholar 

  37. Kim WK, Marcotte EM (2008) Age-dependent evolution of the yeast protein interaction network suggests a limited role of gene duplication and divergence. PLoS Comput Biol 4(11):e1000232

    Article  PubMed  Google Scholar 

  38. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Book  Google Scholar 

  39. Koonin EV (2011) Are there laws of genome evolution? PLoS Comput Biol 7(8):e1002173

    Article  PubMed  CAS  Google Scholar 

  40. Lynch M (2007) The origins of genome architecture. Sinauer Associates, Sunderland

    Google Scholar 

  41. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401

    CAS  Google Scholar 

  42. May RM (2004) Uses and abuses of mathematics in biology. Science 303(5659):790

    Article  PubMed  CAS  Google Scholar 

  43. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, Alon U (2002) Network motifs: simple building blocks of complex networks. Science 298(5594):824

    Article  PubMed  CAS  Google Scholar 

  44. Neyfakh AA, Baranova NN, Mizrokhi LJ (2006) A system for studying evolution of life-like virtual organisms. Biol Direct 1(1):23

    Article  PubMed  Google Scholar 

  45. Pagie L, Hogeweg P (1997) Evolutionary consequences of coevolving targets. Evol Comput 5(4):401–418

    Article  PubMed  Google Scholar 

  46. Pál C, Hurst LD (2003) Evidence for co-evolution of gene order and recombination rate. Nat Genet 33(3):392–395

    Article  PubMed  Google Scholar 

  47. Pastor-Satorras R, Smith E, Solé RV (2003) Evolving protein interaction networks through gene duplication. J Theor Biol 222(2):199–210

    Article  PubMed  CAS  Google Scholar 

  48. Renner A, Bornberg-Bauer E (1997) Exploring the fitness landscapes of lattice proteins. Pac Symp Biocomput 361–372

    Google Scholar 

  49. Romero PA, Arnold FH (2009) Exploring protein fitness landscapes by directed evolution. Nat Rev Mol Cell Biol 10(12):866–876

    Article  PubMed  CAS  Google Scholar 

  50. Savill NJ, Rohandi P, Hogeweg P (1997) Self-reinforcing spatial patterns enslave evolution in a host-parasitoid system. J Theor Biol 188:11–20

    Article  PubMed  CAS  Google Scholar 

  51. Scharloo W (1991) Canalization: genetic and developmental aspects. Annu Rev Ecol Systemat 22:65–93

    Article  Google Scholar 

  52. Schultes EA, Bartel DP (2000) One sequence, two ribozymes: Implications for the emergence of new ribozyme folds. Science 289(5478):448

    Article  PubMed  CAS  Google Scholar 

  53. Schuster P, Fontana W, Stadler PF, Hofacker IL (1994) From sequences to shapes and back: a case study in RNA secondary structures. Proc Biol Sci 255(1344):279–284

    Article  PubMed  CAS  Google Scholar 

  54. Shakhnovich BE, Deeds E, Delisi C, Shakhnovich E (2005) Protein structure and evolutionary history determine sequence space topology. Genome Res 15(3):385

    Article  PubMed  CAS  Google Scholar 

  55. Smith JM, Szathmáry E (1997) The major transitions in evolution. Oxford University Press, Oxford

    Google Scholar 

  56. Takeuchi N, Hogeweg P (2008) Evolution of complexity in RNA-like replicator systems. Biol Direct 3(11). doi:10.1186/1745-6150-3-11

    Google Scholar 

  57. Takeuchi N, Hogeweg P (2009) Multilevel selection in models of prebiotic evolution II: a direct comparison of compartmentalization and spatial self-organization. PLoS Comput Biol 5(10):e1000542

    Article  PubMed  Google Scholar 

  58. Takeuchi N, Poorthuis P, Hogeweg P (2005) Phenotypic error threshold; additivity and epistasis in rna evolution. BMC Evol Biol 5(1):9

    Article  PubMed  Google Scholar 

  59. Takeuchi N, Hogeweg P, Koonin EV (2011) On the origin of dna genomes: evolution of the division of labor between template and catalyst in model replicator systems. PLoS Comput Biol 7(3):e1002024

    Article  PubMed  CAS  Google Scholar 

  60. ten Tusscher K, Hogeweg P (2009) The role of genome and gene regulatory network canalization in the evolution of multi-trait polymorphisms and sympatric speciation. BMC Evol Biol 9(1):159

    Article  PubMed  Google Scholar 

  61. Van Der Laan JD, Hogeweg P (1995) Predator-prey coevolution: Interactions among different time scales. Proc Roy Soc Lond B 259:35–42

    Article  Google Scholar 

  62. Van Hoek MJA, Hogeweg P (2006) In silico evolved lac operons exhibit bistability for artificial inducers, but not for lactose. Biophys J 91(8):2833–2843

    Article  PubMed  Google Scholar 

  63. Van Nimwegen E, Crutchfield JP (2000) Metastable evolutionary dynamics: crossing fitness barriers or escaping via neutral paths? Bull Math Biol 62(5):799–848

    Article  PubMed  Google Scholar 

  64. Van Nimwegen E, Crutchfield JP, Huynen M (1999) Neutral evolution of mutational robustness. Proc Natl Acad Sci USA 96(17):9716

    Article  PubMed  Google Scholar 

  65. Van Noort V, Snel B, Huynen MA (2004) The yeast coexpression network has a small-world, scale-free architecture and can be explained by a simple model. EMBO Rep 5(3):280–284

    Article  PubMed  Google Scholar 

  66. Wagner A (2005) Robustness and evolvability in living systems. Princeton University Press, Princeton

    Google Scholar 

  67. Wagner A (2008) Neutralism and selectionism: a network-based reconciliation. Nat Rev Genet 9(12):965–974

    Article  PubMed  CAS  Google Scholar 

  68. Wagner A (2008) Robustness and evolvability: a paradox resolved. Proc Roy Soc B Biol Sci 275(1630):91

    Article  Google Scholar 

  69. Wagner A (2011) The origins of evolutionary innovations: a theory of transformative change in living systems. Oxford University Press, Oxford

    Google Scholar 

  70. Wloch DM, Szafraniec K, Borts RH, Korona R (2001) Direct estimate of the mutation rate and the distribution of fitness effects in the yeast saccharomyces cerevisiae. Genetics 159(2):441

    PubMed  CAS  Google Scholar 

  71. Wright S (1932) The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc 6th Int Cong Genet 1:356–366

    Google Scholar 

  72. Zuckerkandl E (1997) Neutral and nonneutral mutations: the creative mix; evolution of complexity in gene interaction systems. J Mol Evol 44:2–8

    Article  Google Scholar 

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Acknowledgements

I thank my (former) students, in particular Nobuto Takeuchi, Anton Crombach, Otto Corderro, and Thomas Cuypers. I reviewed their work in this chapter, and I thoroughly enjoyed working with them! I also thank my longtime collaborator Ben Hesper for his strong conceptual support.

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Hogeweg, P. (2012). Toward a Theory of Multilevel Evolution: Long-Term Information Integration Shapes the Mutational Landscape and Enhances Evolvability. In: Soyer, O. (eds) Evolutionary Systems Biology. Advances in Experimental Medicine and Biology, vol 751. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3567-9_10

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