Skip to main content
Log in

Mutation Rate Evolution in Replicator Dynamics

  • Original Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

The mutation rate of an organism is itself evolvable. In stable environments, if faithful replication is costless, theory predicts that mutation rates will evolve to zero. However, positive mutation rates can evolve in novel or fluctuating environments, as analytical and empirical studies have shown. Previous work on this question has focused on environments that fluctuate independently of the evolving population. Here we consider fluctuations that arise from frequency-dependent selection in the evolving population itself. We investigate how the dynamics of competing traits can induce selective pressure on the rates of mutation between these traits. To address this question, we introduce a theoretical framework combining replicator dynamics and adaptive dynamics. We suppose that changes in mutation rates are rare, compared to changes in the traits under direct selection, so that the expected evolutionary trajectories of mutation rates can be obtained from analysis of pairwise competition between strains of different rates. Depending on the nature of frequency-dependent trait dynamics, we demonstrate three possible outcomes of this competition. First, if trait frequencies are at a mutation–selection equilibrium, lower mutation rates can displace higher ones. Second, if trait dynamics converge to a heteroclinic cycle—arising, for example, from “rock-paper-scissors” interactions—mutator strains succeed against non-mutators. Third, in cases where selection alone maintains all traits at positive frequencies, zero and nonzero mutation rates can coexist indefinitely. Our second result suggests that relatively high mutation rates may be observed for traits subject to cyclical frequency-dependent dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Notes

  1. Perhaps contrary to intuition, the value of σ x is in general undefined on the individual fixed points of such a heteroclinic cycle. This is because, if v is a fixed point on this cycle, and if all fixed points are hyperbolic—the generic case—then σ x ({v}) will not converge according to the limit definition (1) (Gaunersdorfer 1992; Sigmund 1992). Thus, according to our definition, the singleton {v} is a non-measurable subset, as is any proper subset of the vertex set. However, this does not affect our current argument, which requires only that the entire vertex set is assigned probability one.

References

  • Aharoni, A., Gaidukov, L., Khersonsky, O., Gould, S. M. Q., Roodveldt, C., & Tawfik, D. S. (2005). The ‘evolvability’ of promiscuous protein functions. Nat. Genet., 37(1), 73–76.

    Google Scholar 

  • André, J.-B., & Godelle, B. (2006). The evolution of mutation rate in finite asexual populations. Genetics, 172(1), 611–626.

    Article  Google Scholar 

  • Bonneuil, N. (1992). Attractors and confiners in demography. Ann. Oper. Res., 37, 17–32.

    Article  MathSciNet  MATH  Google Scholar 

  • Brandstrom, M., & Ellegren, H. (2007). The genomic landscape of short insertion and deletion polymorphisms in the chicken (Gallus gallus) genome: a high frequency of deletions in tandem duplicates. Genetics, 176, 1691–1701.

    Article  Google Scholar 

  • Buss, L. W., & Jackson, J. B. C. (1979). Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat., 113(2), 223–234.

    Article  Google Scholar 

  • Chen, J. Q., Wu, Y., Yang, H., Bergelson, J., Kreitman, M., & Tian, D. (2009). Variation in the ratio of nucleotide substitution and indel rates across genomes in mammals and bacteria. Mol. Biol. Evol., 26, 1523–1531.

    Article  Google Scholar 

  • Chen, F., Liu, W.-Q., Eisenstark, A., Johnston, R., Liu, G.-R., & Liu, S.-L. (2010). Multiple genetic switches spontaneously modulating bacterial mutability. BMC Evol. Biol., 10(1), 277.

    Article  Google Scholar 

  • Chicone, C. C. (2006). Ordinary differential equations with applications. Berlin: Springer.

    MATH  Google Scholar 

  • Cortez, M. H., & Ellner, S. P. (2010). Understanding rapid evolution in predator–prey interactions using the theory of fast–slow dynamical systems. Am. Nat., 176(5), e109–e127.

    Article  Google Scholar 

  • Dercole, F. (2002). Evolutionary dynamics through bifurcation analysis: methods and applications. Ph.D. thesis, Department of Electronics and Information, Politecnico di Milano, Milano, Italy.

  • Dercole, F., & Rinaldi, S. (2008). Analysis of evolutionary processes: the adaptive dynamics approach and its applications. Princeton: Princeton University Press.

    MATH  Google Scholar 

  • Dercole, F., Ferrière, R., Gragnani, A., & Rinaldi, S. (2006). Coevolution of slow–fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex Red Queen dynamics. Proc. R. Soc. B, Biol. Sci., 273, 983–990. 1589.

    Article  Google Scholar 

  • Desai, M. M., & Fisher, D. S. (2011). The balance between mutators and nonmutators in asexual populations. Genetics, 188(4), 997–1014.

    Article  Google Scholar 

  • Dieckmann, U., & Law, R. (1996). The dynamical theory of coevolution: a derivation from stochastic ecological processes. J. Math. Biol., 34(5), 579–612.

    Article  MathSciNet  MATH  Google Scholar 

  • Dieckmann, U., Marrow, P., & Law, R. (1995). Evolutionary cycling in predator–prey interactions: population dynamics and the Red Queen. J. Theor. Biol., 176(1), 91–102.

    Article  Google Scholar 

  • Doebeli, M. (1995). Evolutionary predictions from invariant physical measures of dynamic processes. J. Theor. Biol., 173(4), 377–387.

    Article  MathSciNet  Google Scholar 

  • Doebeli, M., & Koella, J. C. (1995). Evolution of simple population dynamics. Proc. R. Soc. B, Biol. Sci., 260(1358), 119–125.

    Article  Google Scholar 

  • Duret, L. (2009). Mutation patterns in the human genome: more variable than expected. PLoS Biol., 7, e1000028.

    Article  Google Scholar 

  • Earl, D. J., & Deem, M. W. (2004). Evolvability is a selectable trait. Proc. Natl. Acad. Sci., 101(32), 11531–11536.

    Article  Google Scholar 

  • Eckmann, J. P., & Ruelle, D. (1985). Ergodic theory of chaos and strange attractors. Rev. Mod. Phys., 57(3), 617–656.

    Article  MathSciNet  Google Scholar 

  • Elango, N., Kim, S. H., Program, N. C. S., Vigoda, E., & Soojin, V. Y. (2008). Mutations of different molecular origins exhibit contrasting patterns of regional substitution rate variation. PLoS Comput. Biol., 4, e1000015.

    Article  Google Scholar 

  • Fryxell, K. J., & Moon, W. J. (2005). CpG mutation rates in the human genome are highly dependent on local GC content. Mol. Biol. Evol., 22, 650–658.

    Article  Google Scholar 

  • Gaunersdorfer, A. (1992). Time averages for heteroclinic attractors. SIAM J. Appl. Math., 52(5), 1476–1489.

    Article  MathSciNet  MATH  Google Scholar 

  • Geritz, S. A. H. (2005). Resident–invader dynamics and the coexistence of similar strategies. J. Math. Biol., 50(1), 67–82.

    Article  MathSciNet  MATH  Google Scholar 

  • Geritz, S. A. H., Kisdi, E., Meszeńa, G., & Metz, J. A. J. (1997). Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol., 12(1), 35–57.

    Article  Google Scholar 

  • Geritz, S. A. H., Gyllenberg, M., Jacobs, F. J. A., & Parvinen, K. (2002). Invasion dynamics and attractor inheritance. J. Math. Biol., 44, 548–560.

    Article  MathSciNet  MATH  Google Scholar 

  • Giraud, A., Matic, I., Tenaillon, O., Clara, A., Radman, M., Fons, M., & Taddei, F. (2001). Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science, 291(5513), 2606–2608.

    Article  Google Scholar 

  • Gore, J., Youk, H., & Van Oudenaarden, A. (2009). Snowdrift game dynamics and facultative cheating in yeast. Nature, 458(7244), 253–256.

    Article  Google Scholar 

  • Gyllenberg, M., Osipov, A., & Söderbacka, G. (1996). Bifurcation analysis of a metapopulation model with sources and sinks. J. Nonlinear Sci., 6, 329–366.

    Article  MathSciNet  MATH  Google Scholar 

  • Hadeler, K. P. (1981). Stable polymorphisms in a selection model with mutation. SIAM J. Appl. Math., 41(1), 1–7.

    Article  MathSciNet  Google Scholar 

  • Heino, M., Metz, J. A. J., & Kaitala, V. (1998). The enigma of frequency-dependent selection. Trends Ecol. Evol., 13(9), 367–370.

    Article  Google Scholar 

  • Hodgkinson, A., Ladoukakis, E., & Eyre-Walker, A. (2009). Cryptic variation in the human mutation rate. PLoS Biol., 7, e1000027.

    Article  Google Scholar 

  • Hofbauer, J. (1985). The selection mutation equation. J. Math. Biol., 23(1), 41–53.

    Article  MathSciNet  MATH  Google Scholar 

  • Hofbauer, J. (1994). Heteroclinic cycles in ecological differential equations. Tatra Mt. Math. Publ., 4, 105–116.

    MathSciNet  MATH  Google Scholar 

  • Hofbauer, J., & Sigmund, K. (1990). Adaptive dynamics and evolutionary stability. Appl. Math. Lett., 3(4), 75–79.

    Article  MathSciNet  MATH  Google Scholar 

  • Hofbauer, J., & Sigmund, K. (1998). Evolutionary games and replicator dynamics. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Hofbauer, J., & Sigmund, K. (2003). Evolutionary game dynamics. Bull. Am. Math. Soc., 40(4), 479–520.

    Article  MathSciNet  MATH  Google Scholar 

  • Hofbauer, J., Schuster, P., & Sigmund, K. (1979). A note on evolutionary stable strategies and game dynamics. J. Theor. Biol., 81(3), 609–612.

    Article  MathSciNet  Google Scholar 

  • Horn, R. A., & Johnson, C. R. (1990). Matrix analysis. Cambridge: Cambridge University Press.

    MATH  Google Scholar 

  • Ishii, K., Matsuda, H., Iwasa, Y., & Sasaki, A. (1989). Evolutionarily stable mutation rate in a periodically changing environment. Genetics, 121, 163–174.

    Google Scholar 

  • Johnson, T. (1999a). Beneficial mutations, hitchhiking and the evolution of mutation rates in sexual populations. Genetics, 151(4), 1621–1631.

    Google Scholar 

  • Johnson, T. (1999b). The approach to mutation–selection balance in an infinite asexual population, and the evolution of mutation rates. Proc. R. Soc. B, Biol. Sci., 266(1436), 2389–2397.

    Article  Google Scholar 

  • Kerr, B., Riley, M. A., Feldman, M. W., & Bohannan, B. J. M. (2002). Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature, 418(6894), 171–174.

    Article  Google Scholar 

  • Kessler, D. A., & Levine, H. (1998). Mutator dynamics on a smooth evolutionary landscape. Phys. Rev. Lett., 80, 2012–2015.

    Article  Google Scholar 

  • Khibnik, A. I., & Kondrashov, A. S. (1997). Three mechanisms of red queen dynamics. Proc. R. Soc. Lond. B, Biol. Sci., 264(1384), 1049–1056.

    Article  Google Scholar 

  • Kimura, M. (1967). On the evolutionary adjustment of spontaneous mutation rates. Genet. Res., 9, 23–34.

    Article  Google Scholar 

  • King, D. G., Soller, M., & Kashi, Y. (1997). Evolutionary tuning knobs. Endeavour, 21, 36–40.

    Article  Google Scholar 

  • Kirkup, B. C., & Riley, M. A. (2004). Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature, 428(6981), 412–414.

    Article  Google Scholar 

  • Kirschner, M., & Gerhart, J. (1998). Evolvability. Proc. Natl. Acad. Sci. USA, 95(15), 8420–8427.

    Article  Google Scholar 

  • Krivan, V., & Cressman, R. (2009). On evolutionary stability in prey–predator models with fast behavioral dynamics. Evol. Ecol. Res., 11, 227–251.

    Google Scholar 

  • Leigh, E. G. (1970). Natural selection and mutability. Am. Nat., 104, 301–305.

    Article  Google Scholar 

  • Leigh, E. G. (1973). The evolution of mutation rates. Genetics, 73, 1–18.

    MathSciNet  Google Scholar 

  • Levinson, G., & Gutman, G. A. (1987a). High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res., 15, 5323–5338.

    Article  Google Scholar 

  • Levinson, G., & Gutman, G. A. (1987b). Slipped-strand mispairing: a major mechanism for DNA evolution. Mol. Biol. Evol., 4, 203–221.

    Google Scholar 

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

    Google Scholar 

  • Magnus, J. R., & Neudecker, H. (1988). Matrix differential calculus with applications in statistics and econometrics. New York: Wiley.

    MATH  Google Scholar 

  • Marrow, P., Law, R., & Cannings, C. (1992). The coevolution of predator–prey interactions: ESSs and red queen dynamics. Proc. R. Soc. Lond. B, Biol. Sci., 250(1328), 133–141.

    Article  Google Scholar 

  • May, R. M. (1972). Limit cycles in predator–prey communities. Science, 177(4052), 900–902.

    Article  Google Scholar 

  • May, R. M. (2001). Stability and complexity in model ecosystems. Princeton: Princeton University Press.

    MATH  Google Scholar 

  • May, R. M., & Leonard, W. J. (1975). Nonlinear aspects of competition between three species. SIAM J. Appl. Math., 29(2), 243–253.

    Article  MathSciNet  MATH  Google Scholar 

  • Maynard Smith, J., & Price, G. R. (1973). The logic of animal conflict. Nature, 246(5427), 15–18.

    Article  Google Scholar 

  • Metz, J. A. J., Nisbet, R. M., & Geritz, S. A. H. (1992). How should we define ‘fitness’ for general ecological scenarios? Trends Ecol. Evol., 7(6), 198–202.

    Article  Google Scholar 

  • Metz, J. A. J., Geritz, S. A. H., Meszéna, G., Jacobs, F. A., & van Heerwaarden, J. S. (1996). Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction. In S. J. van Strien & S. M. V. Lunel (Eds.), Stochastic and spatial structures of dynamical systems (pp. 183–231). Amsterdam: KNAW Verhandelingen, Afd.

    Google Scholar 

  • Milinski, M. (1987). Tit for tat in sticklebacks and the evolution of cooperation. Nature, 325(6103), 433–435.

    Article  Google Scholar 

  • Murphy, G. L., Connell, T. D., Barritt, D. S., Koomey, M., & Cannon, J. G. (1989). Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell, 56, 539–547.

    Article  Google Scholar 

  • Nowak, M. A. (2006). Five rules for the evolution of cooperation. Science, 314(5805), 1560–1563.

    Article  Google Scholar 

  • Nowak, M. A., & Sigmund, K. (2004). Evolutionary dynamics of biological games. Science, 303(5659), 793–799.

    Article  Google Scholar 

  • Nowak, M. A., Komarova, N. L., & Niyogi, P. (2001). Evolution of universal grammar. Science, 291(5501), 114–118.

    Article  MathSciNet  MATH  Google Scholar 

  • Oliver, A., Cantón, R., Campo, P., Baquero, F., & Blázquez, J. (2000). High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science, 288(5469), 1251.

    Article  Google Scholar 

  • Orr, H. A. (2000). The rate of adaptation in asexuals. Genetics, 155(2), 961–968.

    Google Scholar 

  • Paquin, C. E., & Adams, J. (1983). Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature, 368–371.

  • Pigliucci, M., & Box, P. (2008). Is evolvability evolvable? Nat. Rev. Genet., 9, 75–82.

    Article  Google Scholar 

  • Radman, M., Matic, I., & Taddei, F. (1999). Evolution of evolvability. Ann. N.Y. Acad. Sci., 870(1), 146–155.

    Article  Google Scholar 

  • Rainey, P. B., & Rainey, K. (2003). Evolution of cooperation and conflict in experimental bacterial populations. Nature, 425(6953), 72–74.

    Article  Google Scholar 

  • Rand, D. A., Wilson, H. B., & McGlade, J. M. (1994). Dynamics and evolution: evolutionarily stable attractors, invasion exponents and phenotype dynamics. Philos. Trans. R. Soc. B, Biol. Sci., 343(1305), 261–283.

    Article  Google Scholar 

  • Rosche, W., Foster, P., & Cairns, J. (1999). The role of transient hypermutators in adaptive mutation in Escherichia coli. Proc. Natl. Acad. Sci., 96, 6862–6867.

    Article  Google Scholar 

  • Ruelle, D. (1989). Chaotic evolution and strange attractors. Cambridge: Cambridge University Press.

    Book  MATH  Google Scholar 

  • Schnabl, W., Stadler, P. F., Forst, C., & Schuster, P. (1991). Full characterization of a strange attractor. Physica D, 48(1), 65–90.

    Article  MathSciNet  MATH  Google Scholar 

  • Schuster, P., & Sigmund, K. (1983). Replicator dynamics. J. Theor. Biol., 100(533), 8.

    MathSciNet  Google Scholar 

  • Seger, J., & Antonovics, J. (1988). Dynamics of some simple host–parasite models with more than two genotypes in each species [and discussion]. Philos. Trans. R. Soc. B, 319(1196), 541–555.

    Article  Google Scholar 

  • Shaver, A. C., & Sniegowski, P. D. (2003). Spontaneously arising mutl mutators in evolving Escherichia coli populations are the result of changes in repeat length. J. Bacteriol., 185(20), 6076–6079.

    Article  Google Scholar 

  • Sigmund, K. (1992). Time averages for unpredictable orbits of deterministic systems. Ann. Oper. Res., 37, 217–228. doi:10.1007/BF02071057.

    Article  MathSciNet  MATH  Google Scholar 

  • Sinervo, B., & Calsbeek, R. (2006). The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu. Rev. Ecol. Evol. Syst., 37, 581–610.

    Article  Google Scholar 

  • Sinervo, B., & Lively, C. M. (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240–243.

    Article  Google Scholar 

  • Sinervo, B., Miles, D. B., Frankino, W. A., Klukowski, M., & DeNardo, D. F. (1996). Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm. Behav., 38, 222–233.

    Article  Google Scholar 

  • Sniegowski, P. D., Gerrish, P. J., & Lenski, R. E. (1997). Evolution of high mutation rates in experimental populations of Escherichia coli. Nature, 387(6634), 703–705.

    Article  Google Scholar 

  • Sniegowski, P. D., Gerrish, P. J., Johnson, T., & Shaver, A. (2000). The evolution of mutation rates: separating causes from consequences. BioEssays, 22(12), 1057–1066.

    Article  Google Scholar 

  • Taddei, F., Radman, M., Maynard Smith, J., Toupance, B., Gouyon, P. H., & Godelle, B. (1997). Role of mutator alleles in adaptive evolution. Nature, 387(6634), 700–702.

    Article  Google Scholar 

  • Takens, F. (1985). On the numerical determination of the dimension of an attractor. In B. Braaksma, H. Broer, & F. Takens (Eds.), Lecture notes in mathematics: Vol. 1125. Dynamical systems and bifurcations (pp. 99–106). Berlin: Springer.

    Chapter  Google Scholar 

  • Taylor, P. D., & Jonker, L. B. (1978). Evolutionary stable strategies and game dynamics. Math. Biosci., 40(1–2), 145–156.

    Article  MathSciNet  MATH  Google Scholar 

  • Tenaillon, O., Toupance, B., Le Nagard, H., Taddei, F., & Godelle, B. (1999). Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics, 152(2), 485–493.

    Google Scholar 

  • Tian, D., Wang, Q., Zhang, P., Araki, H., Yang, S., Kreitman, M., Nagylaki, T., Hudson, R., Bergelson, J., & Chen, J. Q. (2008). Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature, 455, 105–108.

    Article  Google Scholar 

  • Travis, J. M. J., & Travis, E. R. (2002). Mutator dynamics in fluctuating environments. Proc. R. Soc. B, Biol. Sci., 269(1491), 591–597.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Weber, M. (1996). Evolutionary plasticity in prokaryotes: a Panglossian view. Biol. Philos., 11, 67–88.

    Article  Google Scholar 

  • Woods, R. J., Barrick, J. E., Cooper, T. F., Shrestha, U., Kauth, M. R., & Lenski, R. E. (2011). Second-order selection for evolvability in a large Escherichia coli population. Science, 331(6023), 1433–1436.

    Article  Google Scholar 

  • Wylie, C. S., Ghim, C., Kessler, D., & Levine, H. (2009). The fixation probability of rare mutators in finite asexual populations. Genetics, 181, 1595–1612.

    Article  Google Scholar 

  • Zhao, Z., & Jiang, C. (2007). Methylation-dependent transition rates are dependent on local sequence lengths and genomic regions. Mol. Biol. Evol., 24, 23–25.

    Article  MathSciNet  Google Scholar 

Download references

Acknowledgements

We thank Yaneer Bar-Yam, David Fried, Glen R. Hall, Aaron Hoffman, Yoh Iwasa, Christopher J. Marx, Martin A. Nowak, Mike Todd, Mary Wahl, John Wakeley, C. Scott Wylie, and an anonymous referee for insightful discussions and comments. Financial support was provided by the National Science Foundation Graduate Research Fellowship Program (D.I.S.R.) and the Foundational Questions in Evolutionary Biology initiative of the John Templeton Foundation (B.A.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Benjamin Allen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Allen, B., Rosenbloom, D.I.S. Mutation Rate Evolution in Replicator Dynamics. Bull Math Biol 74, 2650–2675 (2012). https://doi.org/10.1007/s11538-012-9771-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-012-9771-8

Keywords

Navigation