Abstract
Plasticity-led evolution is a form of evolution where a change in the environment induces novel traits via phenotypic plasticity, after which the novel traits are genetically accommodated over generations under the novel environment. This mode of evolution is expected to resolve the problem of gradualism (i.e., evolution by the slow accumulation of mutations that induce phenotypic variation) implied by the Modern Evolutionary Synthesis, in the face of a large environmental change. While experimental works are essential for validating that plasticity-led evolution indeed happened, we need computational models to gain insight into its underlying mechanisms and make qualitative predictions. Such computational models should include the developmental process and gene-environment interactions in addition to genetics and natural selection. We point out that gene regulatory network models can incorporate all the above notions. In this review, we highlight results from computational modelling of gene regulatory networks that consolidate the criteria of plasticity-led evolution. Since gene regulatory networks are mathematically equivalent to artificial recurrent neural networks, we also discuss their analogies and discrepancies, which may help further understand the mechanisms underlying plasticity-led evolution.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bergman A, Siegal ML (2003) Evolutionary capacitance as a general feature of complex gene networks. Nature 424(6948):549–552. https://doi.org/10.1038/nature01765
Bishop CM (2006) Pattern recognition and machine learning. Springer, New York
Broom M, Rychtár J (2013) Game-theoretical models in biology. CRC Press, Boca Raton
Chevin LM, Lande R (2010) When do adaptive plasticity and genetic evolution prevent extinction of a density-regulated population? Evolution 64(4):1143–1150. https://doi.org/10.1111/j.1558-5646.2009.00875.x
Chevin LM, Leung C, Le Rouzic A, et al. (2022) Using phenotypic plasticity to understand the structure and evolution of the genotype–phenotype map. Genetica 150(3):209–221. https://doi.org/10.1007/s10709-021-00135-5
Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row Publishers, New York. reprinted in 2009 by Blackburn Press
Draghi JA, Whitlock MC (2012) Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66(9):2891–2902. https://doi.org/10.1111/j.1558-5646.2012.01649.x
Ehrenreich IM, Pfennig DW (2016) Genetic assimilation: a review of its potential proximate causes and evolutionary consequences. Ann Bot 117(5):769–779. https://doi.org/10.1093/aob/mcv130
Emlen DJ (1997) Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagusacuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41(5):335–341. https://doi.org/10.1007/s002650050393
Espinosa-Soto C (2016) Selection for distinct gene expression properties favours the evolution of mutational robustness in gene regulatory networks. J Evol Biol 29(11):2321–2333. https://doi.org/10.1111/jeb.12959
Espinosa-Soto C, Wagner A (2010) Specialization can drive the evolution of modularity. PLoS Comput Biol 6(3):e1000,719. https://doi.org/10.1371/journal.pcbi.1000719
Espinosa-Soto C, Hernández U, Posadas-García YS (2021) Recombination facilitates genetic assimilation of new traits in gene regulatory networks. Evol Dev 23(5):459–473. https://doi.org/10.1111/ede.12391
Espinosa-Soto C, Martin OC, Wagner A (2011a) Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol Biol 11(1):1–14. https://doi.org/10.1186/1471-2148-11-5
Espinosa-Soto C, Martin OC, Wagner A (2011b) Phenotypic robustness can increase phenotypic variability after nongenetic perturbations in gene regulatory circuits. J Evol Biol 24(6):1284–1297. https://doi.org/10.1111/j.1420-9101.2011.02261.x
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. 4th edn. Pearson, Harlow
Fierst JL (2011) A history of phenotypic plasticity accelerates adaptation to a new environment. J Evol Biol 24(9):1992–2001. https://doi.org/10.1111/j.1420-9101.2011.02333.x
Gerhart J, Kirschner M (2007) The theory of facilitated variation. Proc Natl Acad Sci USA 104(suppl 1):8582–8589. https://doi.org/10.1073/pnas.0701035104
Ghalambor CK, Hoke KL, Ruell EW, et al. (2015) Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525(7569):372–375. https://doi.org/10.1038/nature15256
Gilbert SF, Epel D (2009) Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer Associates, Sunderland
Hangartner S, Sgrò CM, Connallon T, et al. (2022) Sexual dimorphism in phenotypic plasticity and persistence under environmental change: an extension of theory and meta-analysis of current data. Ecol Lett. https://doi.org/10.1111/ele.14005
Kaneko T, Kikuchi M (2022) Evolution enhances mutational robustness and suppresses the emergence of a new phenotype: a new computational approach for studying evolution. PLoS Comput Biol 18(1):e1009,796. https://doi.org/10.1371/journal.pcbi.1009796
Kouvaris K, Clune J, Kounios L, et al. (2017) How evolution learns to generalise: using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comput Biol 13 (4):e1005,358. https://doi.org/10.1371/journal.pcbi.1005358
Kovaka K (2020) Underdetermination and evidence in the developmental plasticity debate. Brit J Phil Sci. https://doi.org/10.1093/bjps/axx038
Laland K, Uller T, Feldman M, et al. (2014) Does evolutionary theory need a rethink? Nature 514(7521):161–164. https://doi.org/10.1038/514161a
Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22(7):1435–1446. https://doi.org/10.1111/j.1420-9101.2009.01754.x
Levis NA, Pfennig DW (2016) Evaluating ‘plasticity-first’evolution in nature: key criteria and empirical approaches. Trends Ecol Evol 31(7):563–574. https://doi.org/10.1016/j.tree.2016.03.012
Levis NA, Pfennig DW (2019) Plasticity-led evolution: evaluating the key prediction of frequency-dependent adaptation. Proc R Soc B 286(1897):20182,754. https://doi.org/10.1098/rspb.2018.2754
Levis NA, Pfennig DW (2021) Innovation and diversification via plasticity-led evolution. In: Pfennig DW (ed) Phenotypic plasticity & evolution. CRC Press, Boca Raton, pp 211–240. https://doi.org/10.1201/9780429343001-9
Masel J (2004) Genetic assimilation can occur in the absence of selection for the assimilating phenotype, suggesting a role for the canalization heuristic. J Evol Biol 17(5):1106–1110. https://doi.org/10.1111/j.1420-9101.2004.00739.x
Masel J (2005) Evolutionary capacitance may be favored by natural selection. Genet 170 (3):1359–1371. https://doi.org/10.1534/genetics.105.040493
Masel J (2013) Q&A: evolutionary capacitance. BMC Biol 11(1):1–4. https://doi.org/10.1186/1741-7007-11-103
Maynard Smith J (1998) Evolutionary genetics. Oxford University Press, New York
Merilä J, Laurila A, Lindgren B (2004) Variation in the degree and costs of adaptive phenotypic plasticity among rana temporaria populations. J Evol Biol 17(5):1132–1140. https://doi.org/10.1111/j.1420-9101.2004.00744.x
Müller GB (2007) Evo–devo: extending the evolutionary synthesis. Nat Rev Genet 8(12):943–949. https://doi.org/10.1038/nrg2219
Nagata S, Kikuchi M (2020) Emergence of cooperative bistability and robustness of gene regulatory networks. PLoS Comput Biol 16(6):e1007,969. https://doi.org/10.1371/journal.pcbi.1007969
Nishikawa K, Kinjo AR (2014) Cooperation between phenotypic plasticity and genetic mutations can account for the cumulative selection in evolution. Biophysics 10:99–108. https://doi.org/10.2142/biophysics.10.99
Nishikawa K, Kinjo AR (2018) Mechanism of evolution by genetic assimilation: equivalence and independence of genetic mutation and epigenetic modulation in phenotypic expression. Biophys Rev 10(2):667–676. https://doi.org/10.1007/s12551-018-0403-x
Nowak MA (2006) Evolutionary dynamics: exploring the equations of life. Harvard University Press, Cambridge
Parter M, Kashtan N, Alon U (2008) Facilitated variation: how evolution learns from past environments to generalize to new environments. PLoS Comput Biol 4(11):e1000,206. https://doi.org/10.1371/journal.pcbi.1000206
Pfennig DW (2021) Phenotypic plasticity & evolution: causes, consequences, controversies. CRC Press, Boca Raton. https://doi.org/10.1201/9780429343001
Rago A, Kouvaris K, Uller T, et al. (2019) How adaptive plasticity evolves when selected against. PLoS Comput Biol 15(3):e1006,260. https://doi.org/10.1371/journal.pcbi.1006260
Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396(6709):336–342. https://doi.org/10.1038/24550
Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Evol Syst, pp 35–68. https://doi.org/10.2307/2097172
Scheiner SM, Levis NA (2021) The loss of phenotypic plasticity via natural selection: genetic assimilation. In: Phenotypic plasticity & evolution. CRC Press, Boca Raton, pp 161-181. https://doi.org/10.1201/9780429343001-7
Scheiner SM, Barfield M, Holt RD (2020) The genetics of phenotypic plasticity. xvii. response to climate change. Evol Appl 13(2):388–399. https://doi.org/10.1111/eva.12876
Schneider RF, Li Y, Meyer A, et al. (2014) Regulatory gene networks that shape the development of adaptive phenotypic plasticity in a cichlid fish. Mol Ecol 23(18):4511–4526. https://doi.org/10.1111/mec.12851
Schulz LC (2010) The dutch hunger winter and the developmental origins of health and disease. Proc Natl Acad Sci USA 107(39):16,757–16,758. https://doi.org/10.1073/pnas.1012911107
Szilágyi A, Szabó P, Santos M, et al. (2020) Phenotypes to remember: evolutionary developmental memory capacity and robustness. PLoS Comput Biol 16(11):e1008,425. https://doi.org/10.1371/journal.pcbi.1008425
Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7:118–126. https://doi.org/10.2307/2405747
Wagner A (1996) Does evolutionary plasticity evolve? Evolution 50(3):1008–1023. https://doi.org/10.1111/j.1558-5646.1996.tb02342.x
Watson RA, Szathmáry E (2016) How can evolution learn? Trends Ecol Evol 31(2):147–157. https://doi.org/10.1016/j.tree.2015.11.009
Watson RA, Wagner GP, Pavlicev M, et al. (2014) The evolution of phenotypic correlations and “developmental memory”. Evolution 68(4):1124–1138. https://doi.org/10.1111/evo.12337
Weiner SA, Toth AL (2012) Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet Res Int 2012:609,810. https://doi.org/10.1155/2012/609810
West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20(1):249–278. https://doi.org/10.1146/annurev.es.20.110189.001341
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
Whiteley SL, Holleley CE, Wagner S, et al. (2021) Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination. PLoS Genet 17(4):e1009,465. https://doi.org/10.1371/journal.pgen.1009465
Acknowledgements
The authors thank David Marshall and Daphne Teck Ching Lai for helpful comments, and Haziq Jamil for stimulating discussion and reading the manuscript.
Author information
Authors and Affiliations
Contributions
E. T. H. N. and A. R. K. reviewed the literature and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ng, E.T.H., Kinjo, A.R. Computational modelling of plasticity-led evolution. Biophys Rev 14, 1359–1367 (2022). https://doi.org/10.1007/s12551-022-01018-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12551-022-01018-5