Abstract
The two related parts of the Conrad Waddington’s proposal, the concepts of canalization and genetic assimilation, formalized yet in the 1940s continue to arouse great interest among professionals, representing one of the most impressive examples of the transdisciplinary development of ideas. Individual development of any organism proceeds in the context of permanent and unavoidable changes in the factors of the external environment and internal perturbations of molecular and physiological processes. Considering that in any population organisms differ genetically, the implementation of the genetic program must therefore be relatively resistant to genetic variability. According to Waddington, individual development is canalized, i.e. occurs within a certain canal of environmental conditions that limits the variability in the developmental trajectory. However, strong environmental changes and considerable internal perturbations are able to “throw” some trajectories outside the walls of this canal. As a result, aberrant phenotypes may emerge, with some of them being able to get involved in subsequent selection. If the conditions that systematically lead to such an aberrant development persist, the features of these phenotypes can be fixed genetically by selection after a few generations. In other words, selection leads to the emergence of phenotype variants, most genetically suitable to the current circumstances, in which developmental trajectories are altered appropriately. Populations of organisms with altered trajectories and different genotypes continue to exist even when the impact of perturbing factors ceases. Waddington called the mechanism underlying the “same phenotype but different genotypes” evolutionary scenario genetic assimilation. Recent outcomes of evolutionary systems biology have provided a quantitative basis for Waddington’s classical concepts on the robustness of individual development and genetic assimilation. It has become possible to further develop these concepts in the light of new experimental results and theoretical ideas. Particular progress has been achieved in analyzing the molecular machinery of canalization. This paper aims to discuss the results obtained in this area of systems biology by computer modeling in comparison with experimental data.
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Notes
Systems biology is a discipline at the intersection of biology and complex systems theory (see https://dic.academic.ru/dic.nsf/ruwiki/1358381).
The genetic background is meant as a constellation of genes interacting with the given gene and influencing the realization of the trait it controls (see https://dic.academic.ru/dic.nsf/medic2/11625).
A cell signaling pathway is considered as a sequence of interacting molecules through which information from a cell receptor is transmitted inside a cell.
Epistasis is a type gene interplay at which alleles of one genes suppress the manifestation of alleles of the other genes.
Ribozyme is a RNA molecule which has catalytic properties.
Homeorhesis is the existence of certain ontogenetic pathways that lead to the emergence of standard phenotypes independently of environmental and genetic impacts (see https://dic.academic.ru).
Creode is a structurally robust way living systems develop. This notion was introduced by C. Waddington (1940) to describe one of the major properties of developing systems, the ability to retain a typical developmental ocurse (or its outcome) in the presence of considerable natural or artificial perturbations, e.g., sharp fluctuations of environmental conditions (see https://dic.academic.ru).
REFERENCES
Schmalhausen, I.I., Factors of Evolution: The Theory of Stabilizing Selection, Chicago, 1949.
Waddington, C.H., The Strategy of the Genes. A Discussion of Some Aspects of Theoretical Biology, London, 1957.
Rendel, J.M., Canalization of the acute phenotype of Drosophila, Evolution, 1959, vol. 13, pp. 425–439. doi: 10.1111/j.1558-5646.1959.tb03033.x
Baldwin, J.M., A new factor in evolution, Am. Nat., 1896, vol. 30, pp. 441–451, 536–553.
Suzuki, Y. and Nijhout, H.F., Evolution of a polyphenism by genetic accommodation, Science, 2006, vol. 311(5761), pp. 650–652. doi: 10.1126/science.1118888
Rutherford, S.L. and Lindquist, S., Hsp90 as a capacitor for morphological evolution, Nature, 1998, vol. 396, pp. 336–342. doi: 10.1038/24550
Siegal, M.L. and Leu, J.Y., On the nature and evolutionary impact of phenotypic robustness mechanisms, Annu. Rev. Ecol., Evolut. Syst., 2014, vol. 45, pp. 496–517. doi: 10.1146/annurev-ecolsys-120213-091705
Lee, C.E. and Gelembiuk, G.W., Evolutionary origins of invasive populations, Evol. Appl., 2008, vol. 1, pp. 427–448. doi: 10.1111/j.1752-4571.2008.00039.x
Rohner, N., Jarosz, D.F., Kowalko, J.E., Yoshizawa, M., Jeffery, W.R, Borowsky, R.L., Lindquist, S., and Tabin, C.J., Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish, Science, 2013, vol. 342, pp. 1372–1375. doi: 10.1126/science.1240276
Hall, M.C., Dworkin, I., Ungerer, M.C., and Purugganan, M., Genetics of microenvironmental canalization in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp. 13717–13722. doi: 10.1073/pnas.0701936104
Chapman, L.J., Galis, F., and Shinn, J., Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid, Ecol. Lett., 2000, vol. 3(5), pp. 387–393. doi: 10.1046/j.1461-0248.2000.00160.x
Siegal, M.L. and Bergman, A., Waddington's canalization revisited: developmental stability and evolution, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 10528–10532. doi: 10.1073/pnas.102303999
Espinosa-Soto, C., Martin, O.C., and Wagner, A., Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits, BMC Evol. Biol., 2011a, vol. 11, 5. doi: 10.1186/1471-2148-11-5
Iwasaki, W.M., Tsuda, M.E., and Kawata, M., Genetic and environmental factors affecting cryptic variations in gene regulatory networks, BMC Evol. Biol., 2013. doi: 10.1186/1471-2148-13-91
Lande, R., Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation, J. Evol. Biol., 2009, vol. 22, pp. 1435–1446. doi: 10.1111/j.1420-9101.2009.01754.x
Fierst, J.L., A history of phenotypic plasticity accelerates adaptation to a new environment, J. Evol. Biol., 2011, vol. 24, pp. 1992–2001. doi: 10.1111/j.1420-9101.2011.02333.x
Spirov, A. and Holloway, D., Using EA to study the evolution of GRNs controlling biological development, Evolutionary Algorithms in Gene Regulatory Network Research, Noman, N. and Iba, H., Eds., 2015, Wiley Interscience, pp. 240–268. doi: 10.1002/9781119079453.ch10
Spirov, A.V., Sabirov, M.A., and Holloway, D.M., Systems evolutionary biology of Waddington's canalization and genetic assimilation, Evolutionary Physiology and Biochemistry – Advances and Perspectives, Levchenko, V.F., Ed., InTech Press, 2018, pp. 167–185. doi: 10.1111/j.1558-5646.2007.00203.x
Ancel, L. and Fontana, W., Plasticity, evolvability and modularity in RNA, J. Exp. Zool., 2000, vol. 288, pp. 242–283.
Hayden, E.J., Ferrada, E., and Wagner, A., Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme, Nature, 2011, vol. 474, pp. 92–95. doi: 10.1038/nature10083
Thom, R., Stabilité structurelle et morphogenèse, InterÉditions, Paris, 1972.
Waddington, C.H., Canalization of development and the inheritance of acquired characters, Nature, 1942, vol. 150, pp. 563–565. doi: 10.1038/150563a0
Waddington, C.H., Genetic assimilation of the bithorax phenotype, Evolution, 1956, vol. 10, pp. 1–13. doi: 0.1111/j.1558-5646.1956.tb02824.x
Wagner, A., The role of robustness in phenotypic adaptation and innovation, Proc. Biol. Sci., 2012, vol. 279, pp. 1249–1258. doi: 10.1098/rspb.2011.2293
Waddington, C.H., Basic biological concepts, Na puti k teoreticheskoi biologii, I. Prolegomena (Towards a Theoretical Biology, vol. I, Waddington, C.H., Ed., Edinburgh, 1968–1972), Astaurov, B.L., Ed., Moscow, 1970.
Gilbert, S.F., Epigenetic landscaping: Waddington’s use of cell fate bifurcation diagrams, Biol. Philos., 1991, vol. 6, pp. 135–154. doi: 10.1007/BF02426835
Slack, J.M.M., Conrad Hal Waddington: the last Renaissance biologist? Nature Reviews Genetics, 2002, vol. 3, pp. 889–695. doi: 10.1038/nrg933
Jamniczky, H.A., Boughner, J.C., Rolian, C., Gonzalez, P.N., Powell, C.D., Schmidt, E.J., Parsons, T.E., Bookstein, F.L., and Hallgrímsson, B., Rediscovering Waddington in the post-genomic age. Operationalising Waddington’s epigenetics reveals new ways to investigate the generation and modulation of phenotypic variation, Bioessays, 2010, vol. 32, pp. 1–6. doi: 10.1002/bies.200900189
Zheng, J., Payne, J.L., and Wagner, A., Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks, Science, 2019, vol. 365(6451), pp. 347–353. doi: 10.1126/science.aax1837
Masel, J. and Trotter, M.V., Robustness and Evolvability, Trends Genet., 2010, vol. 26(9), pp. 406–414. doi: 10.1016/j.tig.2010.06.002
Pigliucci, M. and Murren, C.J., Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution, 2003, vol. 57(7), pp. 1455–1464. doi: 10.1111/j.0014-3820.2003.tb00354.x
Masel, J. and Siegal, M.L., Robustness: mechanisms and consequences, Trends Genet., 2009, vol. 25(9), pp. 395–403. doi: 10.1016/j.tig.2009.07.005
Braendle, C. and Felix, M.A., Plasticity and errors of a robust developmental system in different environments, Dev. Cell, 2008, vol. 15, pp. 714–724. doi: 10.1016/j.devcel.2008.09.011
Kelly, M., Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2019, vol. 374(1768), 20180176. doi: 10.1098/rstb.2018.0176
Levis, N.A. and Pfennig, D.W., Plasticity-led evolution: a survey of developmental mechanisms and empirical tests, Evol. Dev., 2019, doi: 10.1111/ede.12309
Price, T. and Sol, D., Introduction: genetics of colonizing species, Am. Nat., 2008, vol. 172, pp. S1–S3. doi: 10.1086/588639
Aubret, F. and Shine, R., Genetic assimilation and the postcolonization erosion of phenotypic plasticity in island tiger snakes, Curr. Biol., 2009, vol. 19, pp. 1932–1936. doi: 10.1016/j.cub.2009.09.061
Wagner, G.P., Booth, G., and Bagheri-Chaichian, H., A population genetic theory of canalization, Evolution, 1997, vol. 51, pp. 329–347. doi: 10.1111/j.1558-5646.1997.tb02420.x
Masel, J., Genetic assimilation can occur in the absence of selection for the assimilating phenotype, suggesting a role for the canalization heuristic, J. Evol. Biol., 2004, vol. 17(5), pp. 1106–1110. doi: 10.1111/j.1420-9101.2004.00739.x
Palmer, A.R., Symmetry breaking and the evolution of development, Science, 2004, vol. 306(5697), pp. 828–833. doi: 10.1126/science.1103707
Falconer, D.S. and Mackay, T.F.C., Introduction to Quantitative Genetics, Essex, 1996.
Timofeev-Ressovsky, N.V., Vorontsov, N.N., and Yablokov, A.V., Kratkiy ocherk teorii evolutsii (A Brief Essay on Evolution Theory), Moscow, 1977.
Lande, R., Evolution of phenotypic plasticity in colonizing species, Mol. Ecol., 2015. doi: 10.1111/mec.13037
Simpson, G.G., The Baldwin effect, Evolution, 1953, vol. 7, pp. 110–117. doi: 10.1111/j.1558-5646.1953.tb00069.x
Tikhonov, D. and Zhorov, B., Methods of molecular modeling in studies of ion channels and their modulation by ligands, Russ. J. Physiol., 2019, vol. 105, pp. 1333–1348. doi: 10.1134/S0869813919110116
Hayden, E.J. and Wagner, A., Environmental change exposes beneficial epistatic interactions in a catalytic RNA, Proc. R. Soc. B, 2012, vol. 279, pp. 3418–3425. doi: 10.1098/rspb.2012.0956
Spirov, A.V. and Holloway, D.M., New approaches to designing genes by evolution in the computer, Real-World Applications of Genetic Algorithms, Roeva, O., Ed., InTech Press, 2012. doi: 10.5772/36817
Spirov, A.V. and Holloway, D.M., Using evolutionary computations to understand the design and evolution of gene and cell regulatory networks, Methods, 2013, vol. 62, pp. 39–55. doi: 10.1016/j.ymeth.2013.05.013
Wagner, A., Does evolutionary plasticity evolve? Evolution, 1996, vol. 50, pp. 1008–1023. doi: 10.1111/j.1558-5646.1996.tb02342.x
Gavrilets, S. and Hastings, A., A quantitative-genetic model for selection on developmental noise, Evolution, 1994, vol. 48, pp. 1478–1486. doi: 10.1111/j.1558-5646.1994.tb02190.x
Jablonka, E. and Lamb, M.J., Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life, MIT Press, 2005.
Dickens, T. and Rahman, Q., The extended evolutionary synthesis and the role of soft inheritance in evolution, Proc. Biol. Sci., 2012, vol. 279(1740), pp. 2913–2921. doi: 10.1098/rspb.2012.0273
Jablonka, E. and Noble, D., Systemic integration of different inheritance systems, Curr. Opin. Systems Biol., 2019, vol. 13, pp. 52–58. doi: 10.1016/j.coisb.2018.10.002
Waddington, C.H., The epigenotype (1942), Int. J. Epidemiol., 2012, vol. 41(1), pp. 10–13. doi: 10.1093/ije/dyr184
Noble, D., Conrad Waddington and the origin of epigenetics, J. Exp. Biol., 2015, vol. 218, pp. 816–818. doi: 10.1242/jeb.120071
Duclos, K.K., Hendrikse, J.L., and Jamniczky, H.A., Investigating the evolution and development of biological complexity under the framework of epigenetics, Evol. Dev., 2019, e12301. doi: 10.1111/ede.12301
Cavalli, G. and Heard, E., Advances in epigenetics link genetics to the environment and disease, Nature, 2019, vol. 571, pp. 489–499. doi: 10.1038/s41586-019-1411-0
Kotolupov, V.A. and Levchenko, V.F., Multifunctionality and homeostasis. Regularities of the body's functioning important for maintaining homeostasis, J. Evol. Biochem. Physiol., 2009, vol. 45, pp. 91–99. doi: 10.1134/S0022093009040148
Ozernyuk, N.D. and Isaeva, V.V., Evolyutsiya ontogeneza (Evolution of Ontogenesis), Moscow, 2016.
Thom, R., Comments. Dynamic theory of morphogenesis, Na puti k teoreticheskoi biologii, I. Prolegomena (Towards a Theoretical Biology, vol. I, Waddington, C.H., Ed., Edinburgh, 1968–1972), Astaurov, B.L., Ed., Moscow, 1970.
Kriegman, S., Cheney, N., and Bongard, J., How morphological development can guide evolution, Sci. Rep., 2018, vol. 8(1), 13934. doi: 10.1038/s41598-018-31868-7
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Studies covered in review subdivisions 4 and 5 were implemented within the State assignment by the Federal Agency for Scientific Organizations (FASO Russia); project no. 01201351572. Studies described in the other subdivision were supported by the Russian Scientific Foundation grant no. 17-18-01536.
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Translated by A. Polyanovsky
The original online version of this article was revised: the issue date is not January 2020, but January 2021
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Spirov, A.V., Levchenko, V.F. & Sabirov, M.A. Concepts of Canalization and Genetic Assimilation in Developmental Biology: Current Approaches and Studies. J Evol Biochem Phys 57, 1–15 (2021). https://doi.org/10.1134/S0022093021010014
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DOI: https://doi.org/10.1134/S0022093021010014