1932

Abstract

The limits of evolution have long fascinated biologists. However, the causes of evolutionary constraint have remained elusive due to a poor mechanistic understanding of studied phenotypes. Recently, a range of innovative approaches have leveraged mechanistic information on regulatory networks and cellular biology. These methods combine systems biology models with population and single-cell quantification and with new genetic tools, and they have been applied to a range of complex cellular functions and engineered networks. In this article, we review these developments, which are revealing the mechanistic causes of epistasis at different levels of biological organization—in molecular recognition, within a single regulatory network, and between different networks—providing first indications of predictable features of evolutionary constraint.

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2020-05-06
2024-10-13
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Literature Cited

  1. 1. 
    Aguilar-Rodriguez J, Payne JL, Wagner A 2017. A thousand empirical adaptive landscapes and their navigability. Nat. Ecol. Evol. 1:245
    [Google Scholar]
  2. 2. 
    Amell A, Roso-Llorach A, Palomero L, Cuadras D, Galván-Femenía I et al. 2018. Disease networks identify specific conditions and pleiotropy influencing multimorbidity in the general population. Sci. Rep. 8:15970
    [Google Scholar]
  3. 3. 
    Bachmann H, Molenaar D, Branco Dos Santos F, Teusink B 2017. Experimental evolution and the adjustment of metabolic strategies in lactic acid bacteria. FEMS Microbiol. Rev. 41:Supp_1S201–19
    [Google Scholar]
  4. 4. 
    Balleza E, López-Bojorguez LN, Martínez-Antonio A, Resendis-Antonio O, Lozada-Chávez I et al. 2009. Regulation by transcription factors in bacteria: beyond description. FEMS Microbiol. Rev. 33:1133–51
    [Google Scholar]
  5. 5. 
    Beardmore RE, Gudelj I, Lipson DA, Hurst LD 2011. Metabolic trade-offs and the maintenance of the fittest and the flattest. Nature 472:7343342–46
    [Google Scholar]
  6. 6. 
    Bell MA, Futuyma DJ, Eanes WF, Levinton JS 2010. Evolution since Darwin: The First 150 Years Sunderland, MA: Sinauer Assoc.
    [Google Scholar]
  7. 7. 
    Boucher B, Jenna S. 2013. Genetic interaction networks: better understand to better predict. Front. Genet. 4:290
    [Google Scholar]
  8. 8. 
    Bridgham JT, Carroll SM, Thornton JW 2006. Evolution of hormone-receptor complexity by molecular exploitation. Science 312:577097–101
    [Google Scholar]
  9. 9. 
    Carlborg O, Haley CS. 2004. Epistasis: too often neglected in complex trait studies. Nat. Rev. Genet. 5:8618–25
    [Google Scholar]
  10. 10. 
    Carter AJ, Nguyen AQ. 2011. Antagonistic pleiotropy as a widespread mechanism for the maintenance of polymorphic disease alleles. BMC Med. Genet. 12:160
    [Google Scholar]
  11. 11. 
    Cooper VS, Lenski RE. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:6805736–39
    [Google Scholar]
  12. 12. 
    Corson F, Siggia ED. 2012. Geometry, epistasis, and developmental patterning. PNAS 109:155568–75
    [Google Scholar]
  13. 13. 
    Cotterell J, Sharpe J. 2013. Mechanistic explanations for restricted evolutionary paths that emerge from gene regulatory networks. PLOS ONE 8:4e61178
    [Google Scholar]
  14. 14. 
    de Visser JA, Krug J 2014. Empirical fitness landscapes and the predictability of evolution. Nat. Rev. Genet. 15:7480–90
    [Google Scholar]
  15. 15. 
    de Vos MGJ, Dawid A, Sunderlikova V, Tans SJ 2015. Breaking evolutionary constraint with a tradeoff ratchet. PNAS 112:4814906–11
    [Google Scholar]
  16. 16. 
    de Vos MGJ, Poelwijk FJ, Battich N, Ndika JDT, Tans SJ 2013. Environmental dependence of genetic constraint. PLOs Genet 9:6e1003580
    [Google Scholar]
  17. 17. 
    de Vos MGJ, Schoustra SE, de Visser JAGM 2018. Ecology dictates evolution? About the importance of genetic and ecological constraints in adaptation. EPL 122:558002
    [Google Scholar]
  18. 18. 
    Dill KA, Ghosh K, Schmit JD 2011. Physical limits of cells and proteomes. PNAS 108:4417876–82
    [Google Scholar]
  19. 19. 
    Diss G, Lehner B. 2018. The genetic landscape of a physical interaction. eLife 7:e32472
    [Google Scholar]
  20. 20. 
    Fisher RAS. 1930. The Genetical Theory of Natural Selection Oxford, UK: Clarendon Press
    [Google Scholar]
  21. 21. 
    Flynn KM, Cooper TF, Moore FB-G, Cooper VS 2013. The environment affects epistatic interactions to alter the topology of an empirical fitness landscape. PLOS Genet 9:4e1003426
    [Google Scholar]
  22. 22. 
    Gavrilets S, Hastings A. 1993. Maintenance of genetic variability under strong stabilizing selection: a two-locus model. Genetics 134:1377–86
    [Google Scholar]
  23. 23. 
    Gorter FA, Aarts MGM, Zwaan BJ, de Visser JAGM 2018. Local fitness landscapes predict yeast evolutionary dynamics in directionally changing environments. Genetics 208:1307–22
    [Google Scholar]
  24. 24. 
    Gros PA, Le Nagard H, Tenaillon O 2009. The evolution of epistasis and its links with genetic robustness, complexity and drift in a phenotypic model of adaptation. Genetics 182:1277–93
    [Google Scholar]
  25. 25. 
    Halatek J, Brauns F, Frey E 2018. Self-organization principles of intracellular pattern formation. Philos. Trans. R. Soc. Lond. B 373:174720170107
    [Google Scholar]
  26. 26. 
    Hill WG, Zhang XS. 2012. Assessing pleiotropy and its evolutionary consequences: Pleiotropy is not necessarily limited, nor need it hinder the evolution of complexity. Nat. Rev. Genet 13:4296 Author reply. 2012. Nat. Rev. Genet. 13(4):296
    [Google Scholar]
  27. 27. 
    Hottes AK, Freddolino PL, Khare A, Donnell ZN, Liu JC, Tavazoie S 2013. Bacterial adaptation through loss of function. PLOS Genet 9:7e1003617
    [Google Scholar]
  28. 28. 
    Jerison ER, Kryazhimskiy S, Mitchell JK, Bloom JS, Kruglyak L, Desai MM 2017. Genetic variation in adaptability and pleiotropy in budding yeast. eLife 6:e27167
    [Google Scholar]
  29. 29. 
    Kassen R, Rainey PB. 2004. The ecology and genetics of microbial diversity. Annu. Rev. Microbiol. 58:207–31
    [Google Scholar]
  30. 30. 
    Koch EN, Costanzo M, Deshpande R, Andrews B, Boone C, Myers CL 2017. Systematic identification of pleiotropic genes from genetic interactions. bioRxiv 112326. https://doi.org/10.1101/112326
    [Crossref]
  31. 31. 
    Laan L, Koschwanez JH, Murray AW 2015. Evolutionary adaptation after crippling cell polarization follows reproducible trajectories. eLife 4:e09638
    [Google Scholar]
  32. 32. 
    Lagator M, Paixão T, Barton NH, Bollback JP, Guet CC 2017. On the mechanistic nature of epistasis in a canonical cis-regulatory element. eLife 6:e25192
    [Google Scholar]
  33. 33. 
    Lagator M, Sarikas S, Acar H, Bollback JP, Guet CC 2017. Regulatory network structure determines patterns of intermolecular epistasis. eLife 6:e28921
    [Google Scholar]
  34. 34. 
    Lehming N, Sartorius J, Kisters-Woike B, von Wilcken-Bergmann B, Müller-Hill B 1990. Mutant lac repressors with new specificities hint at rules for protein–DNA recognition. EMBO J 9:3615–21
    [Google Scholar]
  35. 35. 
    Lehner B. 2011. Molecular mechanisms of epistasis within and between genes. Trends Genet 27:8323–31
    [Google Scholar]
  36. 36. 
    Li C, Zhang J. 2018. Multi-environment fitness landscapes of a tRNA gene. Nat. Ecol. Evol. 2:61025–32
    [Google Scholar]
  37. 37. 
    Lindsey HA, Gallie J, Taylor S, Kerr B 2013. Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494:7438463–67
    [Google Scholar]
  38. 38. 
    Lobkovsky AE, Koonin EV. 2012. Replaying the tape of life: quantification of the predictability of evolution. Front. Genet. 3:246
    [Google Scholar]
  39. 39. 
    Lunzer M, Miller SP, Felsheim R, Dean AM 2005. The biochemical architecture of an ancient adaptive landscape. Science 310:5747499–501
    [Google Scholar]
  40. 40. 
    MacLean RC, Bell G, Rainey PB 2004. The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. . PNAS 101:218072–77
    [Google Scholar]
  41. 41. 
    Martin G. 2014. Fisher's geometrical model emerges as a property of complex integrated phenotypic networks. Genetics 197:1237–55
    [Google Scholar]
  42. 42. 
    Martin G, Elena SF, Lenormand T 2007. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nat. Genet. 39:4555–60
    [Google Scholar]
  43. 43. 
    Martin SG. 2015. Spontaneous cell polarization: Feedback control of Cdc42 GTPase breaks cellular symmetry. Bioessays 37:111193–201
    [Google Scholar]
  44. 44. 
    Moore JH. 2003. The ubiquitous nature of epistasis in determining susceptibility to common human diseases. Hum. Hered. 56:1–373–82
    [Google Scholar]
  45. 45. 
    Mustonen V, Lassig M. 2009. From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation. Trends Genet 25:3111–19
    [Google Scholar]
  46. 46. 
    Nghe P, Kogenaru M, Tans SJ 2018. Sign epistasis caused by hierarchy within signalling cascades. Nat. Commun. 9:1451
    [Google Scholar]
  47. 47. 
    Orr HA. 2000. Adaptation and the cost of complexity. Evolution 54:113–20
    [Google Scholar]
  48. 48. 
    Peng W, Liu P, Xue Y, Acar M 2015. Evolution of gene network activity by tuning the strength of negative-feedback regulation. Nat. Commun. 6:16226
    [Google Scholar]
  49. 49. 
    Peter IS, Davidson EH. 2011. Evolution of gene regulatory networks controlling body plan development. Cell 144:6970–85
    [Google Scholar]
  50. 50. 
    Phillips PC. 2008. Epistasis: the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 9:11855–67
    [Google Scholar]
  51. 51. 
    Podgornaia AI, Laub MT. 2015. Protein evolution: pervasive degeneracy and epistasis in a protein-protein interface. Science 347:6222673–77
    [Google Scholar]
  52. 52. 
    Poelwijk FJ, de Vos MGJ, Tans SJ 2011. Tradeoffs and optimality in the evolution of gene regulation. Cell 146:3462–70
    [Google Scholar]
  53. 53. 
    Poelwijk FJ, Heyning PD, de Vos MGJ, Kiviet DJ, Tans SJ 2011. Optimality and evolution of transcriptionally regulated gene expression. BMC Syst. Biol. 5:128
    [Google Scholar]
  54. 54. 
    Poelwijk FJ, Kiviet DJ, Weinriech DM, Tans SJ 2007. Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445:7126383–86
    [Google Scholar]
  55. 55. 
    Poelwijk FJ, Socolich M, Ranganathan R 2019. Learning the pattern of epistasis linking genotype and phenotype in a protein. Nat. Commun. 10:4213
    [Google Scholar]
  56. 56. 
    Poelwijk FJ, Taňase-Nicola S, Kiviet DJ, Tans SJ 2011. Reciprocal sign epistasis is a necessary condition for multi-peaked fitness landscapes. J. Theor. Biol. 272:1141–44
    [Google Scholar]
  57. 57. 
    Prud'homme B, Gompel N, Carroll SB 2007. Emerging principles of regulatory evolution. PNAS 104:Suppl. 18605–12
    [Google Scholar]
  58. 58. 
    Qian W, Ma D, Xiao C, Wang Z, Zhang J 2012. The genomic landscape and evolutionary resolution of antagonistic pleiotropy in yeast. Cell Rep 2:51399–410
    [Google Scholar]
  59. 59. 
    Rojas Echenique JI, Kryazhimskiy S, Nguyen Ba AN, Desai MM 2019. Modular epistasis and the compensatory evolution of gene deletion mutants. PLOS Genet 15:2e1007958
    [Google Scholar]
  60. 60. 
    Sartorius J, Lehming N, Kisters B, von Wilcken-Bergmann B, Müller-Hill B 1989. lac repressor mutants with double or triple exchanges in the recognition helix bind specifically to lac operator variants with multiple exchanges. EMBO J 8:41265–70
    [Google Scholar]
  61. 61. 
    Schaerli Y, Jiménez A, Duarte JM, Mihajlovic L, Renggli J et al. 2018. Synthetic circuits reveal how mechanisms of gene regulatory networks constrain evolution. Mol. Syst. Biol. 14:9e8102
    [Google Scholar]
  62. 62. 
    Segrè D, Deluna A, Church GM, Kishony R 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37:177–83
    [Google Scholar]
  63. 63. 
    Slaughter BD, Unruh JR, Das A, Smith SE, Rubinstein B, Li R 2013. Non-uniform membrane diffusion enables steady-state cell polarization via vesicular trafficking. Nat. Commun. 4:1380
    [Google Scholar]
  64. 64. 
    Sorrells TR, Booth LN, Tuch BB, Johnson AD 2015. Intersecting transcription networks constrain gene regulatory evolution. Nature 523:7560361–65
    [Google Scholar]
  65. 65. 
    Starr TN, Picton LK, Thornton JW 2017. Alternative evolutionary histories in the sequence space of an ancient protein. Nature 549:7672409–13
    [Google Scholar]
  66. 66. 
    Starr TN, Thornton JW. 2016. Epistasis in protein evolution. Protein Sci 25:71204–18
    [Google Scholar]
  67. 67. 
    Stearns FW. 2010. One hundred years of pleiotropy: a retrospective. Genetics 186:3767–73
    [Google Scholar]
  68. 68. 
    Steinberg B, Ostermeier M. 2016. Environmental changes bridge evolutionary valleys. Sci. Adv. 2:1e1500921
    [Google Scholar]
  69. 69. 
    Szamecz B, Boross G, Kalapis D, Kovács K, Fekete G et al. 2014. The genomic landscape of compensatory evolution. PLOS Biol 12:8e1001935
    [Google Scholar]
  70. 70. 
    Szathmáry E. 1993. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics 133:1127–32
    [Google Scholar]
  71. 71. 
    Tyler AL, Crawford DC, Pendergrass SA 2016. The detection and characterization of pleiotropy: discovery, progress, and promise. Brief Bioinform 17:113–22
    [Google Scholar]
  72. 72. 
    Voordeckers K, Pougach K, Verstrepen KJ 2015. How do regulatory networks evolve and expand throughout evolution. Curr. Opin. Biotechnol. 34:180–88
    [Google Scholar]
  73. 73. 
    Wagner GP, Zhang J. 2011. The pleiotropic structure of the genotype-phenotype map: the evolvability of complex organisms. Nat. Rev. Genet. 12:3204–13
    [Google Scholar]
  74. 74. 
    Wang Z, Liao BY, Zhang J 2010. Genomic patterns of pleiotropy and the evolution of complexity. PNAS 107:4218034–39
    [Google Scholar]
  75. 75. 
    Weinreich DM, Delaney NF, Depristo MA, Hartl DL 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:5770111–14
    [Google Scholar]
  76. 76. 
    Weinreich DM, Watson RA, Chao L 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:61165–74
    [Google Scholar]
  77. 77. 
    Woods B, Lai H, Wu CF, Zyla TR, Savage NS, Lew DJ 2016. Parallel actin-independent recycling pathways polarize Cdc42 in budding yeast. Curr. Biol. 26:162114–26
    [Google Scholar]
  78. 78. 
    Wright S. 1932. The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proceedings of the Sixth International Congress of Genetics, Vol. 1 DF Jones 356–66 Austin, TX: Genet. Soc. Am.
    [Google Scholar]
  79. 79. 
    Yang YF, Cao W, Wu S, Qian W 2017. Genetic interaction network as an important determinant of gene order in genome evolution. Mol. Biol. Evol. 34:123254–66
    [Google Scholar]
  80. 80. 
    Zhang XS, Hill WG. 2005. Genetic variability under mutation selection balance. Trends Ecol. Evol. 20:9468–70
    [Google Scholar]
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