Plasticity is found in all domains of life and is particularly relevant when populations experience variable environmental conditions. Traditionally, evolutionary models of plasticity are non-mechanistic: they typically view reactions norms as the target of selection, without considering the underlying genetics explicitly. Consequently, there have been difficulties in understanding the emergence of plasticity, and in explaining its limits and costs. In this paper, we offer a novel mechanistic approximation for the emergence and evolution of plasticity. We simulate random "epigenetic mutations" in the genotype-phenotype mapping, of the kind enabled by DNA-methylations/demethylations. The frequency of epigenetic mutations at loci affecting the phenotype is sensitive to organism stress (trait-environment mismatch), but is also genetically determined and evolvable. Thus, the "random motion" of epigenetic markers enables developmental learning-like behaviors that can improve adaptation within the limits imposed by the genotypes. However, with random motion being "goal-less," this mechanism is also vulnerable to developmental noise leading to maladaptation. Our individual-based simulations show that epigenetic mutations can hide alleles that are temporarily unfavorable, thus enabling cryptic genetic variation. These alleles can be advantageous at later times, under regimes of environmental change, in spite of the accumulation of genetic loads. Simulations also demonstrate that plasticity is favored by natural selection in constant environments, but more under periodic environmental change. Plasticity also evolves under directional environmental change as long as the pace of change is not too fast and costs are low.

Czech Academy of Sciences Biology Centre Institute of Entomology České Budějovice Czech Republic

Department of Mathematics Faculty of Science University of South Bohemia České Budějovice Czech Republic

Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The Netherlands

Institute for Botany and Landscape Ecology University of Greifswald Greifswald Germany

Zoological Institute and Museum University of Greifswald Greifswald Germany

Zobrazit více v PubMed

Adrian-Kalchhauser, I., Sultan, S. E., Shama, L. N., Spence-Jones, H., Tiso, S., Valsecchi, C. I. K., & Weissing, F. J. (2020). Understanding “non-genetic” inheritance: Insights from molecular-evolutionary crosstalk. Trends in Ecology & Evolution, 35(12):1078–1089. PubMed

Anderson, G. M. (2005). Thermodynamics of natural systems. Cambridge University Press.

Angers, B., Perez, M., Menicucci, T., & Leung, C. (2020). Sources of epigenetic variation and their applications in natural populations. Evolutionary Applications, 13(6):1262–1278. PubMed PMC

Ashander, J., Chevin, L.-M., & Baskett, M. L. (2016). Predicting evolutionary rescue via evolving plasticity in stochastic environments. Proceedings of the Royal Society B: Biological Sciences, 283(1839):20161690. PubMed PMC

Barton, N. H., Etheridge, A. M., & Véber, A. (2017). The infinitesimal model: Definition, derivation, and implications. Theoretical Population Biology, 118:50–73. PubMed

Berrigan, D., & Scheiner, S. M. (2004). Modeling the evolution of phenotypic plasticity. Phenotypic plasticity: Functional and conceptual approaches (pp. 82–97). New York, NY, Oxford University Press.

Botero, C. A., Weissing, F. J., Wright, J., & Rubenstein, D. R. (2015). Evolutionary tipping points in the capacity to adapt to environmental change. Proceedings of the National Academy of Sciences of the USA, 112(1):184–189. PubMed PMC

Brun-Usan, M., Rago, A., Thies, C., Uller, T., & Watson, R. A. (2020a). Developmental models reveal the role of phenotypic plasticity in explaining genetic evolvability. bioRxiv.

Brun-Usan, M., Thies, C., & Watson, R. A. (2020b). How to fit in: The learning principles of cell differentiation. PLoS Computational Biology, 16(4):e1006811. PubMed PMC

Bürger, R., & Krall, C. (2004). Quantitative-genetic models and changing environments. In Ferrière R., Dieckmann U., & Couvet D. (Eds.), Evolutionary Conservation Biology (Vol. 4, pp. 171–187). Cambridge University Press.

Bürger, R., & Lynch, M. (1995). Evolution and extinction in a changing environment: A quantitative-genetic analysis. Evolution, 49(1):151–163. PubMed

Casadesús, J. (2016). Bacterial DNA methylation and methylomes. In Albert Jeltsch R. Z. J.. (Ed.), DNA methyltransferases-role and function (pp. 35–61). Springer. PubMed

Chevin, L.-M., Lande, R., & Mace, G. M. (2010). Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biology, 8(4):e1000357. PubMed PMC

Curradi, M., Izzo, A., Badaracco, G., & Landsberger, N. (2002). Molecular mechanisms of gene silencing mediated by DNA methylation. Molecular and Cellular Biology, 22(9):3157–3173. PubMed PMC

DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13(2):77–81. PubMed

Duncan, E. J., Cunningham, C. B., & Dearden, P. K. (2022). Phenotypic plasticity: What has DNA methylation got to do with it? Insects, 13(2):110. PubMed PMC

Fallet, M., Luquet, E., David, P., & Cosseau, C. (2020). Epigenetic inheritance and intergenerational effects in mollusks. Gene, 729:144166. PubMed

Foster, P. L. (2007). Stress-induced mutagenesis in bacteria. Critical Reviews in Biochemistry and Molecular Biology, 42(5):373–397. PubMed PMC

Greenberg, M. V. C., & Bourc’his, D. (2019). The diverse roles of DNA methylation in mammalian development and disease. Nature Reviews Molecular Cell Biology, 20(10):590–607. PubMed

Hattman, S., Kenny, C., Berger, L., & Pratt, K. (1978). Comparative study of DNA methylation in three unicellular eucaryotes. Journal of Bacteriology, 135(3):1156–1157. PubMed PMC

Hermisson, J. & Wagner, G. P. (2004). The population genetic theory of hidden variation and genetic robustness. Genetics, 168(4):2271–2284. PubMed PMC

Hildebrandt, J.-P., Bleckmann, H., & Homberg, U. (2021). Penzlin-Lehrbuch der Tierphysiologie. Springer.

Houle, D. (1992). Comparing evolvability and variability of quantitative traits. Genetics, 130(1):195–204. PubMed PMC

Huey, R. B., Hertz, P. E., & Sinervo, B. (2003). Behavioral drive versus behavioral inertia in evolution: A null model approach. The American Naturalist, 161(3):357–366. PubMed

Jablonka, E. (2017). The evolutionary implications of epigenetic inheritance. Interface Focus, 7(5):20160135. PubMed PMC

Kirschner, M. & Gerhart, J. (1998). Evolvability. Proceedings of the National Academy of Sciences, 95(15):8420–8427. PubMed PMC

Kribelbauer, J. F., Lu, X.-J., Rohs, R., Mann, R. S., & Bussemaker, H. J. (2020). Toward a mechanistic understanding of DNA methylation readout by transcription factors. Journal of Molecular Biology, 432(6):1801–1815. PubMed PMC

Laland, K. N., Uller, T., Feldman, M. W., Sterelny, K., Müller, G. B., Moczek, A., Jablonka, E., & Odling-Smee, J. (2015). The extended evolutionary synthesis: Its structure, assumptions and predictions. Proceedings of the Royal Society B: Biological Sciences, 282(1813):20151019. PubMed PMC

Lande, R. (2009). Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology, 22(7):1435–1446. PubMed

Lande, R. (2014). Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment. Journal of Evolutionary Biology, 27(5):866–875. PubMed

Li, E. & Zhang, Y. (2014). DNA methylation in mammals. Cold Spring Harbor Perspectives in Biology, 6(5):a019133. PubMed PMC

Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. (Vol. 1). Sinauer Sunderland, MA.

Massicotte, R. & Angers, B.. (2012). General-purpose genotype or how epigenetics extend the flexibility of a genotype. Genetics Research International, 2012:1–7. PubMed PMC

Moore, L. D., Le, T., & Fan, G. (2013). DNA methylation and its basic function. Neuropsychopharmacology, 38(1):23–38. PubMed PMC

Murren, C. J., Auld, J. R., Callahan, H., Ghalambor, C. K., Handelsman, C. A., Heskel, M. A., Kingsolver, J., Maclean, H. J., Masel, J., Maughan, H., Pfennig, D. W., Relyea, R. A., Seiter, S., Snell-Rood, E., Steiner, U. K., & Schlichting, C. D. (2015). Constraints on the evolution of phenotypic plasticity: Limits and costs of phenotype and plasticity. Heredity, 115(4):293–301. PubMed PMC

Niederhuth, C. E., Bewick, A. J., Ji, L., Alabady, M. S., Kim, K. D., Li, Q., Rohr, N. A., Rambani, A., Burke, J. M., Udall, J. A., Egesi, C., Schmutz, J., Grimwood, J., Jackson, S. A., Springer, N. M., & Schmitz, R. J. (2016). Widespread natural variation of DNA methylation within angiosperms. Genome Biology, 17(1):1–19. PubMed PMC

Nunney, L. (2016). Adapting to a changing environment: Modeling the interaction of directional selection and plasticity. Journal of Heredity, 107(1):15–24. PubMed

Paaby, A. B., & Rockman, M. V. (2014). Cryptic genetic variation: Evolution’s hidden substrate. Nature Reviews Genetics, 15(4):247–258. PubMed PMC

Parsons, K. J., McWhinnie, K., Pilakouta, N., & Walker, L. (2020). Does phenotypic plasticity initiate developmental bias? Evolution & Development, 22(1–2):56–70. PubMed PMC

Pfennig, D. W. (2021). Phenotypic plasticity & evolution: Causes, consequences, controversies. Taylor & Francis.

Pigliucci, M. (2005). Evolution of phenotypic plasticity: Where are we going now? Trends in Ecology & Evolution, 20(9):481–486. PubMed

Reed, T. E., Waples, R. S., Schindler, D. E., Hard, J. J., & Kinnison, M. T. (2010). Phenotypic plasticity and population viability: The importance of environmental predictability. Proceedings of the Royal Society B: Biological Sciences, 277(1699):3391–3400. PubMed PMC

Richards, C. L., Alonso, C., Becker, C., Bossdorf, O., Bucher, E., Colomé-Tatché, M., Durka, W., Engelhardt, J., Gaspar, B., Gogol-Döring, A., Grosse, I., van Gurp, T. P., Heer, K., Kronholm, I., Lampei, C., Latzel, V., Mirouze, M., Opgenoorth, L., Paun, O., Prohaska, S. J., Rensing, S. A., Stadler, P. F., Trucchi, E., Ullrich, K., & Verhoeven, K. J. F. (2017). Ecological plant epigenetics: Evidence from model and non-model species, and the way forward. Ecology Letters, 20(12):1576–1590. PubMed

Richards, E. J. (2006). Inherited epigenetic variation—revisiting soft inheritance. Nature Reviews Genetics, 7(5):395–401. PubMed

Romero-Mujalli, D., Rochow, M., Kahl, S., Paraskevopoulou, S., Folkertsma, R., Jeltsch, F., & Tiedemann, R. (2021). Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies. Ecology and Evolution, 11(11):6341–6357. PubMed PMC

Scheiner, S. M., Barfield, M., & Holt, R. D. (2020). The genetics of phenotypic plasticity. XVII. Response to climate change. Evolutionary Applications, 13(2):388–399. PubMed PMC

Scheiner, S. M. & Holt, R. D. (2012). The genetics of phenotypic plasticity. X. Variation versus uncertainty. Ecology and Evolution, 2(4):751–767. PubMed PMC

Schlichting, C. D., & Wund, M. A. (2014). Phenotypic plasticity and epigenetic marking: An assessment of evidence for genetic accommodation. Evolution, 68(3):656–672. PubMed

Shi, J., Xu, J., Chen, Y. E., Li, J. S., Cui, Y., Shen, L., Li, J. J., & Li, W. (2021). The concurrence of DNA methylation and demethylation is associated with transcription regulation. Nature Communications, 12(1):5285. PubMed PMC

Slotkin, R. K., & Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nature Reviews Genetics, 8(4):272–285. PubMed

Smithson, M., Thorson, J. L., Sadler-Riggleman, I., Beck, D., Skinner, M. K., & Dybdahl, M. (2020). Between-generation phenotypic and epigenetic stability in a clonal snail. Genome Biology and Evolution, 12(9):1604–1615. PubMed PMC

Sommer, R. J. (2020). Phenotypic plasticity: From theory and genetics to current and future challenges. Genetics, 215(1):1–13. PubMed PMC

Symanowski, F., & Hildebrandt, J.-P. (2010). Differences in osmotolerance in freshwater and brackish water populations of Theodoxus fluviatilis (gastropoda: Neritidae) are associated with differential protein expression. Journal of Comparative Physiology B, 180(3):337–346. PubMed

Thibert-Plante, X., & Hendry, A. (2011). The consequences of phenotypic plasticity for ecological speciation. Journal of Evolutionary Biology, 24(2):326–342. PubMed

Thorson, J. L., Smithson, M., Beck, D., Sadler-Riggleman, I., Nilsson, E., Dybdahl, M., & Skinner, M. K. (2017). Epigenetics and adaptive phenotypic variation between habitats in an asexual snail. Scientific Reports, 7(1):1–11. PubMed PMC

Thorson, J. L., Smithson, M., Sadler-Riggleman, I., Beck, D., Dybdahl, M., & Skinner, M. K. (2019). Regional epigenetic variation in asexual snail populations among urban and rural lakes. Environmental Epigenetics, 5(4):dvz020. PubMed PMC

van Gestel, J., & Weissing, F. J. (2016). Regulatory mechanisms link phenotypic plasticity to evolvability. Scientific Reports, 6(1):1–15. PubMed PMC

Wagner, A. (1994). Evolution of gene networks by gene duplications: A mathematical model and its implications on genome organization. Proceedings of the National Academy of Sciences, 91(10):4387–4391. PubMed PMC

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

Wagner, A. (2008). Robustness and evolvability: A paradox resolved. Proceedings of the Royal Society B: Biological Sciences, 275(1630):91–100. PubMed PMC

Watson, R. A. & Szathmáry, E. (2016). How can evolution learn? Trends in Ecology & Evolution, 31(2):147–157. PubMed