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Constraints, Trade-offs and the Currency of Fitness

Abstract

Understanding evolutionary trajectories remains a difficult task. This is because natural evolutionary processes are simultaneously affected by various types of constraints acting at the different levels of biological organization. Of particular importance are constraints where correlated changes occur in opposite directions, called trade-offs. Here we review and classify the main evolutionary constraints and trade-offs, operating at all levels of trait hierarchy. Special attention is given to life history trade-offs and the conflict between the survival and reproduction components of fitness. Cellular mechanisms underlying fitness trade-offs are described. At the metabolic level, a linear trade-off between growth and flux variability was found, employing bacterial genome-scale metabolic reconstructions. Its analysis indicates that flux variability can be considered as the currency of fitness. This currency is used for fitness transfer between fitness components during adaptations. Finally, a discussion is made regarding the constraints which limit the increase in the amount of fitness currency during evolution, suggesting that occupancy constraints are probably the main restrictions.

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References

  1. Acerenza L (1993) Metabolic control design. J Theor Biol 165:63–85

    CAS  Article  PubMed  Google Scholar 

  2. Acerenza L (1996a) How constrained is metabolic control? J Theor Biol 182:277–283

    CAS  Article  PubMed  Google Scholar 

  3. Acerenza L (1996b) Sensitivity constraints in a chemical/biochemical highly responsive system. BioSystems 39:109–116

    CAS  Article  PubMed  Google Scholar 

  4. Acerenza L, Graña M (2006) On the origins of a crowded cytoplasm. J Mol Evol 63:583–590

    CAS  Article  PubMed  Google Scholar 

  5. Acerenza L, Cristina E, Hernández JA (2011) Regulatory design in a simple system integrating membrane potential generation and metabolic ATP consumption. Robustness and the role of energy dissipating processes. Biochim Biophys Acta 1807:1634–1646

    CAS  Article  PubMed  Google Scholar 

  6. Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. In: Bell MA, Eanes WF, Futuyma DJ, Levinton JS (eds) Evolution after Darwin: the first 150 years. Sinauer Associates, Sunderland, pp 243–268

    Google Scholar 

  7. Andersson DI (2014) Evolution of Antibiotic Resistance. In: Losos JB (ed) The Princeton guide to evolution. Princeton University Press, Princeton, pp 747–753

    Google Scholar 

  8. Antonovics J, van Tienderen PH (1991) Ontoecogenophyloconstraints? The chaos of constraint terminology. Trends Ecol Evol 6:166–168

    CAS  Article  PubMed  Google Scholar 

  9. Arnold SJ (1992) Constraints on phenotypic evolution. Am Nat 140:S85–S107

    Article  PubMed  Google Scholar 

  10. Arnold SJ, Pfrender ME, Jones AG (2001) The adaptive landscape as a conceptual bridge between micro and macroevolution. Genetica 112–113:9–32

    Article  PubMed  Google Scholar 

  11. Ashby WR (1956) An introduction to cybernetics. Chapman and Hall, London

    Book  Google Scholar 

  12. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305:1622–1625

    CAS  Article  PubMed  Google Scholar 

  13. Bar-Even A, Flamholz A, Noor E, Milo R (2012) Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nat Chem Biol 8:509–517

    CAS  Article  PubMed  Google Scholar 

  14. Bennett AF, Lenski RE (2007) An experimental test of evolutionary trade-offs during temperature adaptation. P Natl Acad Sci USA 104:8649–8654

    CAS  Article  Google Scholar 

  15. Bochdanovits Z, de Jong G (2004) Antagonistic pleiotropy for life-history traits at the gene expression level. P Roy Soc Lond B 271:S75–S78

    CAS  Article  Google Scholar 

  16. Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant-Microbe Interact 22:487–497

    CAS  Article  PubMed  Google Scholar 

  17. Brakefield PM, Roskam JC (2006) Exploring evolutionary constraints is a task for an integrative evolutionary biology. Am Nat 168:S4–S13

    Article  PubMed  Google Scholar 

  18. Brand MD, Chien LF, Ainscow EK, Rolfe DFS, Porter RK (1994) The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187:132–139

    CAS  Article  PubMed  Google Scholar 

  19. Brodie ED III (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–1298

    Article  Google Scholar 

  20. Brunke S, Hube B (2014) Adaptive prediction as a strategy in microbial infections. PLoS Pathog 10:e1004356

    Article  PubMed  PubMed Central  Google Scholar 

  21. Chang DE, Smalley DJ, Conway T (2002) Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model. Mol Microbiol 45:289–306

    CAS  Article  PubMed  Google Scholar 

  22. Cooper VS, Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:736–739

    CAS  Article  PubMed  Google Scholar 

  23. Endler JA (1980) Natural selection of color patterns in Poecilia reticulata. Evolution 34:76–91

    Article  Google Scholar 

  24. Endler JA (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fish 9:173–190

    Article  Google Scholar 

  25. Farhadifar R, Baer CF, Valfort AC, Andersen EC, Muller-Reichert T, Delattre M, Needleman DJ (2015) Scaling, selection and evolutionary dynamics of the mitotic spindle. Curr Biol 25:732–740

    CAS  Article  PubMed  Google Scholar 

  26. Fischer E, Sauer U (2005) Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat Genet 37:636–640

    CAS  Article  PubMed  Google Scholar 

  27. Futuyma DJ (2005) Evolution. Sinauer Associates Inc., Sunderland

    Google Scholar 

  28. Futuyma DJ, Bennett AF (2009) The importance of experimental studies in evolutionary biology. In: Garland T Jr, Rose MR (eds) Experimental evolution. University of California Press, California

    Google Scholar 

  29. Gardener MR, Ashby WR (1970) Connectance of large dynamic (cybernetic) systems: critical values for stability. Nature 228:784

    Article  Google Scholar 

  30. Goldbeter A (1996) Biochemical oscillations and cellular rhythms. Cambridge University Press, Cambridge

    Book  Google Scholar 

  31. Graña M, Acerenza L (2001) A model combining cell physiology and population genetics to explain Escherichia coli laboratory evolution. BMC Evol Biol 1:12

    Article  PubMed  PubMed Central  Google Scholar 

  32. Green JBA, Sharpe J (2015) Positional information and reaction-diffusion: two big ideas in developmental biology combine. Development 142:1203–1211

    CAS  Article  PubMed  Google Scholar 

  33. Guerreiro R, Besson AA, Bellenger J, Ragot K, Lizard G, Faivre B, Sorci G (2012) Correlational selection on pro- and anti-inflammatory effectors. Evolution 66:3615–3623

    CAS  Article  PubMed  Google Scholar 

  34. Guillaume F, Otto SP (2012) Gene functional trade-offs and the evolution of pleiotropy. Genetics 192:1389–1409

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Handorf T, Ebenhoh O, Heinrich R (2005) Expanding metabolic networks: scopes of compounds, robustness and evolution. J Mol Evol 61:498–512

    CAS  Article  PubMed  Google Scholar 

  36. Haverkorn van Rijsewijk BRB, Nanchen A, Nallet S, Kleijn RJ, Sauer U (2011) Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli. Mol Syst Biol 7:477

    Article  PubMed  PubMed Central  Google Scholar 

  37. Heinrich R, Schuster S (1996) The Regulation of cellular systems. Chapman and Hall, New York

    Book  Google Scholar 

  38. Hoffmann A (2014) Evolutionary limits and constraints. In: Losos JB (ed) The Princeton guide to evolution. Princeton University Press, Princeton, pp 247–252

    Google Scholar 

  39. Hofmeyr JH, Kacser H, van der Merwe KJ (1986) Metabolic control analysis of moiety-conserved cycles. Eur J Biochem 155:631–641

    CAS  Article  PubMed  Google Scholar 

  40. Holder N (1983) Developmental constraints and the evolution of vertebrate limb patterns. J Theor Biol 104:451–471

    CAS  Article  PubMed  Google Scholar 

  41. Hughes BS, Cullum AJ, Bennett AF (2007) Evolutionary adaptation to environmental acidity in experimental lineages of Escherichia coli. Evolution 61:1725–1734

    Article  PubMed  Google Scholar 

  42. Hummert S, Bohl K, Basanta D, Deutsch A, Werner S, Theißen G, Schroeter A, Schuster S (2014) Evolutionary game theory: cells as players. Mol BioSyst 10:3044–3065

    CAS  Article  PubMed  Google Scholar 

  43. Jin DJ, Cagliero C, Zhou YN (2012) Growth rate regulation in Escherichia coli. FEMS Microbiol Rev 36:269–287

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Kacser H, Burns JA (1973) The control of flux. Symp Soc Exp Biol 27:65–104

    CAS  PubMed  Google Scholar 

  45. Karn MN, Penrose LS (1951) Birth weight and gestation time in relation to maternal age, parity, and infant survival. Ann Eugen 16:147–164

    CAS  Article  PubMed  Google Scholar 

  46. Keightley PD, Kacser H (1987) Dominance, pleiotropy and metabolic structure. Genetics 117:319–329

    CAS  PubMed  PubMed Central  Google Scholar 

  47. King EG, Roff DA, Fairbairn DJ (2010) Tradeoff acquisition and allocation in Gryllus firmus: a test of the Y model. J Evol Biol 24:256–264

    Article  PubMed  Google Scholar 

  48. Kottler VA, Fadeev A, Weigel D, Dreyer C (2013) Pigment pattern formation in the guppy, Poecilia reticulata, involves the Kita and Csf1ra receptor tyrosine kinases. Genetics 194:631–646

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334

    Article  Google Scholar 

  50. Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33:402–416

    Article  Google Scholar 

  51. Leiby N, Marx CJ (2014) Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biol 12:e1001789

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lenski RE (1998) Bacterial evolution and the cost of antibiotic resistance. Int Microbiol 1:265–270

    CAS  PubMed  Google Scholar 

  53. Lenski RE, Travisano M (1994) Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. P Natl Acad Sci USA 9:6808–6814

    Article  Google Scholar 

  54. López-Maury L, Marguerat S, Bähler J (2008) Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 9:583–593

    Article  PubMed  Google Scholar 

  55. Lutkenhaus J, Mukherjee A (1996) Cell division. In: Neidhart FC (ed) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM Press, Washington DC, pp 1615–1626

    Google Scholar 

  56. Maad J (2000) Phenotypic selection in hawkmoth-pollinated Platanthera bifolia: targets and fitness surfaces. Evolution 54:112–123

    CAS  PubMed  Google Scholar 

  57. Mahadevan R, Schilling CH (2003) The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metab Eng 5:264–276

    CAS  Article  PubMed  Google Scholar 

  58. Marcusson LL, Frimodt-Møller N, Hughes D (2009) Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 5(8):e1000541

    Article  PubMed  PubMed Central  Google Scholar 

  59. Matyssek R, Schnyder H, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds) (2012) Growth and defence in plants, ecological studies 220. Springer, Berlin

    Google Scholar 

  60. May R (1972) Will a large complex system be stable? Nature 238:413–414

    CAS  Article  PubMed  Google Scholar 

  61. May R (1974) Stability and complexity in model ecosystems. Princeton University Press, Princeton

    Google Scholar 

  62. Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L (1985) Developmental constraints and evolution. Q Rev Biol 60:265–287

    Article  Google Scholar 

  63. Mitchell A, Pilpel Y (2011) A mathematical model for adaptive prediction of environmental changes by microorganisms. P Natl Acad Sci USA 108:7271–7276

    CAS  Article  Google Scholar 

  64. Mitchell A, Romano GH, Groisman B, Yona A, Dekel E, Kupiec M, Dahan O, Pilpel Y (2009) Adaptive prediction of environmental changes by microorganisms. Nature 460:220–224

    CAS  Article  PubMed  Google Scholar 

  65. Novak M, Pfeiffer T, Lenski RE, Sauer U, Bonhoeffer S (2006) Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am Nat 168:242–251

    Article  PubMed  Google Scholar 

  66. Nyström T (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54:855–862

    Article  PubMed  Google Scholar 

  67. Orr HA (2009) Fitness and its role in evolutionary genetics. Nat Rev Genet 10:531–539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  68. Orth JD, Conrad TM, Na J, Lerman JA, Nam H, Feist AM, Palsson BØ (2011) A comprehensive genome-scale reconstruction of Escherichia coli metabolism. Mol Syst Biol 7:535

    Article  PubMed  PubMed Central  Google Scholar 

  69. Oster GF, Murray JD (1989) Pattern formation models and developmental constraints. J Exp Zool 251:186–202

    CAS  Article  PubMed  Google Scholar 

  70. Palsson BØ (2006) Systems biology. Properties of reconstructed networks. Cambridge University Press, New York

    Book  Google Scholar 

  71. Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292:504–507

    CAS  Article  PubMed  Google Scholar 

  72. Pilizota T, Shaevitz JW (2014) Origins of Escherichia coli growth rate and cell shape changes at high external osmolality. Biophys J 107:1962–1969

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Raymond J, Segre D (2006) The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:1764–1767

    CAS  Article  PubMed  Google Scholar 

  74. Reder C (1988) Metabolic control theory: a structural approach. J Theor Biol 135:175–201

    CAS  Article  PubMed  Google Scholar 

  75. Rolfe DFS, Brand MD (1997) The physiological significance of mitochondrial proton leak in animal cells and tissues. Bioscience Rep 17:9–16

    CAS  Article  Google Scholar 

  76. San Román M, Cancela H, Acerenza L (2014) Source and regulation of flux variability in Escherichia coli. BMC Sys Biol 8:67

    Article  Google Scholar 

  77. Schluter D, Nychka D (1994) Exploring fitness surfaces. Am Nat 143:597–616

    Article  Google Scholar 

  78. Shoval O, Sheftel H, Shinar G, Hart Y, Ramote O, Mayo A, Dekel E, Kavanagh K, Alon U (2012) Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. Science 336:1157–1160

    CAS  Article  PubMed  Google Scholar 

  79. Simpson GG (1953) The major features of evolution. Columbia University Press, New York

    Google Scholar 

  80. Sinervo B, Svensson E (1998) Mechanistic and selective causes of life history trade-offs and plasticity. Oikos 83:432–442

    Article  Google Scholar 

  81. Tawfik DS (2014) Accuracy-rate tradeoffs: how do enzymes meet demands of selectivity and catalytic efficiency? Curr Opin Chem Biol 21:73–80

    CAS  Article  PubMed  Google Scholar 

  82. Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M et al (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–636

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. Ulusu NN (2015) Evolution of enzyme kinetic mechanisms. J Mol Evol 80:251–257

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142

    Article  Google Scholar 

  85. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Article  Google Scholar 

  86. Waddington CH (1957) The strategy of the genes. George Allen & Unwin, Crows Nest

    Google Scholar 

  87. Zera AJ, Harshman LG (2001) The physiology of life-history trade-offs in animals. Annu Rev Ecol Syst 32:95–126

    Article  Google Scholar 

  88. Zhuang K, Vemuri GN, Mahadevan R (2011) Economics of membrane occupancy and respiro-fermentation. Mol Syst Biol 7:500

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The author acknowledges support from Programa de Desarrollo de las Ciencias Básicas (PEDECIBA, Montevideo) and Agencia Nacional de Investigación e Innovación (ANII, Montevideo).

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Correspondence to Luis Acerenza.

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Acerenza, L. Constraints, Trade-offs and the Currency of Fitness. J Mol Evol 82, 117–127 (2016). https://doi.org/10.1007/s00239-016-9730-3

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Keywords

  • Evolutionary constraint
  • Evolutionary trade-off
  • Fitness cost
  • Fitness trade-off
  • Life history trade-off
  • Trade-off across environments