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Evolutionary capacitance: theory

Biological systems have a tendency to become robust or canalized to perturbation during evolution. This leads to a buildup of cryptic genetic variation. Cryptic genetic variation may not be 100% hidden, and low residual levels of selection may act as a form of pre-screening. This removes the most deleterious alleles and leaves the remaining variation pre-enriched for potential adaptations (Masel 2006). This enrichment means that the majority of adaptations are likely to stem from cryptic genetic variation, making it of fundamental importance in evolution.

Evolutionary capacitors provide a window into cryptic genetic variation, facilitating its study. Evolutionary capacitors are molecular mechanisms that are able to tap into stocks of cryptic genetic variation. Just as an electronic capacitor stores and releases charge, an evolutionary capacitor stores and releases genetic variation. Examples include the yeast prion [PSI+], regulators of alternative splicing, phase variation and gene conversion. In fact, any complex network can have evolutionary capacitance properties, so capacitance is likely to be widespread.

The main example we study as a model system for evolutionary capacitance is the yeast prion [PSI+]. [PSI+] taps into cryptic stocks of variation beyond stop codons by causing elevated rates of readthrough translation. This can lead to faster adaptation: [PSI+] can lead to faster growth rates in stressful environments (True & Lindquist 2000). Evolutionary capacitors may therefore promote evolvability.

When variation is revealed all at once, most of it is likely to be deleterious, while only a small subset is likely to be adaptive. Selection will act to genetically assimilate this subset. For example, [PSI+] may act as a stopgap mechanism, buying yeast time to find the appropriate stop codon mutation (Giacomelli et al. 2007). Once this has occurred, capacitors such as [PSI+] are reversible, and simply disappear. This leaves the organism with a brand new adaptation but no load of other, deleterious mutations, since these disappear with [PSI+]. This reversibility is one of the factors that make evolutionary capacitance a much more potent promoter of evolvability than elevated mutation rates.

It is one thing for capacitors to promote evolvability, but another for this increased evolvability to itself be the product of natural selection. The evolution of evolvability is difficult, because natural selection acts on present costs, not future benefits. We have constructed stochastic mathematical models that balance the weak constant deleterious effects of capacitance through revealing variation at inappropriate times, the rare strongly advantageous effects of capacitance at times of environmental change, and genetic drift. We found both that evolutionary capacitance is favored by natural selection (Masel 2005; King & Masel 2007; Masel, King & Maughan 2007) and that this is by far the most likely explanation for how the ability to form [PSI+] evolved in the first place (Masel & Bergman 2003).

Our goal in this work is to understand evolutionary capacitance, and the biology of the [PSI+] prion is our guide, but along the way our theoretical models have had broader application to other related areas of evolutionary theory. These have included phenotypic plasticity, epigenetic inheritance systems, bet-hedging, and the mutational degradation of complex traits.

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Publications

  • Rajon, E., & Masel, J. (manuscript submitted). The evolution of clumsy gene expression and its consequences for evolvability.
  • Masel, J., & Lyttle, D. N. (manuscript submitted). The consequences of rare sexual reproduction by means of selfing in an otherwise clonally reproducing species.
  • Masel, J., & Trotter, M. V. (2010). Robustness and Evolvability. Trends in Genetics, 26(9), 406-414. (PubMed)Go to document
  • Masel, J., & Siegal, M. L. (2009). Robustness: mechanisms and consequences. Trends Genet. (PubMed)Go to document (doi)Go to document
  • Lancaster, A. K., Bardill, J. P., True, H. L., & Masel, J. (2010). The Spontaneous Appearance Rate of the Yeast Prion [PSI+] and Its Implications For the Evolution of the Evolvability Properties of the [PSI+] System. Genetics, 184(2), 393-400. (PubMed)Go to document (doi)Go to document
  • Griswold, C. K., & Masel, J. (2009). Complex adaptations can drive the evolution of the capacitor [PSI], even with realistic rates of yeast sex. PLoS Genet, 5(6), 1000517. (PubMed)Go to document (doi)Go to document
  • Lancaster, A. K., & Masel, J. (2009). The evolution of reversible switches in the presence of irreversible mimics. Evolution, 63(9), 2350-62. (PubMed)Go to document (doi)Go to document
  • Masel, J., & Griswold, C. K. (2009). The strength of selection against the yeast prion [PSI+]. Genetics, 181(3), 1057-63. (PubMed)Go to document (doi)Go to document
  • King, O. D., & Masel, J. (2007). The evolution of bet-hedging adaptations to rare scenarios. Theor Pop Biol, 72, 560-575. (PDF) (doi)Go to document
  • Masel, J., King, O. D., & Maughan, H. (2007). The loss of adaptive plasticity during long periods of environmental stasis. Am Nat, 169(1), 38-46. (PubMed)Go to document (doi)Go to document
  • Masel, J. (2006). Cryptic genetic variation is enriched for potential adaptations. Genetics, 172(3), 1985-91. (PDF) (PubMed)Go to document (doi)Go to document
  • Masel, J. (2005). Evolutionary capacitance may be favored by natural selection. Genetics, 170(3), 1359-71. (PDF) (PubMed)Go to document (doi)Go to document
  • Masel, J., & Bergman, A. (2003). The evolution of the evolvability properties of the yeast prion [PSI+]. Evolution, 57(7), 1498-512. (PubMed)Go to document