Mechanism of evolution by genetic assimilation
- 102 Downloads
- 1 Citations
Abstract
Conrad H. Waddington discovered the phenomenon of genetic assimilation through a series of experiments on fruit flies. In those experiments, artificially exerted environmental stress induced plastic phenotypic changes in the fruit flies, but after some generations, the same phenotypic variant started to appear without the environmental stress. Both the initial state (where the phenotypic changes were environmentally induced and plastic) and the final state (where the phenotypic changes were genetically fixed and constitutive) are experimental facts. However, it remains unclear how the environmentally induced phenotypic change in the first generation becomes genetically fixed in the central process of genetic assimilation itself. We have argued that the key to understanding the mechanism of genetic assimilation lies in epigenetics, and proposed the “cooperative model” in which the evolutionary process depends on both genetic and epigenetic factors. Evolutionary simulations based on the cooperative model reproduced the process of genetic assimilation. Detailed analysis of the trajectories has revealed genetic assimilation is a process in which epigenetically induced phenotypic changes are incrementally and statistically replaced with multiple minor genetic mutations through natural selection. In this scenario, epigenetic and genetic changes may be considered as mutually independent but equivalent in terms of their effects on phenotypic changes. This finding rejects the common (and confused) hypothesis that epigenetically induced phenotypic changes depend on genetic mutations. Furthermore, we argue that transgenerational epigenetic inheritance is not required for evolution by genetic assimilation.
Keywords
Epigenome Phenotype-driven evolution Phenotypic plasticity Evo-Devo Evolutionary synthesis SimulationNotes
Compliance with Ethical Standards
Conflict of interests
Ken Nishikawa declares that he has no conflict of interest. Akira R. Kinjo declares that he has no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
References
- Alegria-Torres JA, Baccarelli A, Bollati V (2011) Epigenetics and lifestyle. Epigenomics 3:267–277CrossRefPubMedPubMedCentralGoogle Scholar
- Barton NH, Briggs DEG, Eisen JA, Goldstein DB, Patel NH (2007) Evolution. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
- Breitling LP, Yang R, Kom B, Burwinkel B, Brenner H (2011) Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet 88:450–457CrossRefPubMedPubMedCentralGoogle Scholar
- Cheedipudi S, Gennolet O, Dobeva G (2014) Epigenetic inheritance of cell fates during embryonic development. Front Genet 5:19. https://doi.org/10.3389/fgene.2014.00019 CrossRefPubMedPubMedCentralGoogle Scholar
- Crispo E (2007) The Baldwin effect and genetic assimilation: revisiting two mechanisms evolutionary change mediated by phenotypic plasticity. Evolution 61:2469–2479CrossRefPubMedGoogle Scholar
- Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row Publishers, New York. reprinted in 2009 by Blackburn PressGoogle Scholar
- Feil R, Berger F (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23:192–199CrossRefPubMedGoogle Scholar
- Ferguson-Smith AC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet 12:565–575CrossRefPubMedGoogle Scholar
- Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suñer D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102:10:604–10:609. https://doi.org/10.1073/pnas.0500398102 CrossRefGoogle Scholar
- Gibson G, Dworkin I (2004) Uncovering cryptic genetic variation. Nat Rev Genet 5:681–690CrossRefPubMedGoogle Scholar
- Gilbert S, Epel D (2009) Ecological developmental biology: integrating epigenetics, medicine, and evloution. Sinauer Associates Inc., SunderlandGoogle Scholar
- Goldschmidt RB (1938) Physiological Genetics. McGraw-Hill, New YorkGoogle Scholar
- Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105:17:046–17:049CrossRefGoogle Scholar
- Ietswaart R, Wu Z, Dean C (2012) Flowering time control: another window to the connection between antisense RNA and chromatin. Trends Genet 28:445–453CrossRefPubMedGoogle Scholar
- Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanism, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176CrossRefPubMedGoogle Scholar
- Jones AL, Sung S (2014) Mechanisms underlying epigenetic regulation in Arabidopsis thaliana. Integr Comp Biol 54:61–67CrossRefPubMedPubMedCentralGoogle Scholar
- Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319:1827–1830CrossRefPubMedGoogle Scholar
- Laland K, Uller T, Feldman M, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J, Wray GA, Hoekstra HE, Futuyma DJ, Lenski RE, Mackay TFC, Schluter D, Strassmann JE (2014) Does evolutional theory need a rethink? Nature 514:161–164CrossRefPubMedGoogle Scholar
- Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446. https://doi.org/10.1111/j.1420-9101.2009.01754.x CrossRefPubMedGoogle Scholar
- Lickliter R (2014) Developmental evolution and the origins of phenotypic variation. Biomol Concepts 5:343–352CrossRefPubMedGoogle Scholar
- Lindblom R, Ververis K, Tortorella SM, Karagiannis TC (2015) The early life origin theory in the development of cardiovascular disease and type 2 diabetes. Mol Biol Rep 42:791–797CrossRefPubMedGoogle Scholar
- Lumey LH, Stein AD, Kahn HS, van der Pal-de Bruin KM, Blauw GJ, Zybert PA, Susser ES (2007) Cohort profile: the Dutch Hunger Winter families study. Int J Epidemiol 36:1196–1204CrossRefPubMedGoogle Scholar
- Matsuda R (1987) Animal evolution in changing environments: with special reference to abnormal metamorphosis. Wiley, LondonGoogle Scholar
- Moczek AP (2008) On the origins of novelty in development and evolution. Bioessays 30:432–447CrossRefPubMedGoogle Scholar
- Müller GB (2007) Evo-Devo: extending the evolutionary synthesis. Nat Rev Genet 8:943–949CrossRefPubMedGoogle Scholar
- Müller GB, Newman SA (2005) The innovation triad: an EvoDevo agenda. J Exp Zool B Mol Dev Evol 304:487–503CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- Nishikawa K, Kinjo AR (2017) Essential role of long non-coding RNAs in de novo chromatin modifications: the genomic address code hypothesis. Biophys Rev 9:73–77. https://doi.org/10.1007/s12551-017-0259-5 CrossRefPubMedPubMedCentralGoogle Scholar
- Ohta K (2013) Epigenome and Life. Kodansha, TokyoGoogle Scholar
- Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25:459–467. https://doi.org/10.1016/j.tree.2010.05.006 CrossRefPubMedGoogle Scholar
- Pigliucci M (2003) Epigenetics is back! Hsp90 and phenotypic variation. Cell Cycle 2:34–35CrossRefPubMedGoogle Scholar
- Pigliucci M, Müller GB (eds) (2010) Evolution, the extended synthesis. MIT Press, CambridgeGoogle Scholar
- Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B. Biol Sci 270:1433–1440CrossRefGoogle Scholar
- Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093CrossRefPubMedGoogle Scholar
- Roseboom T, de Rooij S, Painter R (2006) The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82:485–491CrossRefPubMedGoogle Scholar
- Roseboom TJ, Painter RC, van Abeelen AF, Veenendaal MV, de Rooij SR (2011) Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 70:141–145CrossRefPubMedGoogle Scholar
- Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342CrossRefPubMedGoogle Scholar
- Sandoval J, Esteller M (2012) Cancer epigenomics: beyond genomics. Curr Opin Genet Develop 22:50–55CrossRefGoogle Scholar
- Sawarkar R, Paro R (2013) Hsp90@chromatin.nucleus: an emerging hub of a networker. Trends Cell Biol 23:193–201CrossRefPubMedGoogle Scholar
- Scharloo W (1991) Canalization: genetic and developmental aspects. Annu Rev Ecol Syst 22:65–93CrossRefGoogle Scholar
- Schlichting CD, Wund MA (2014) Phenotypic plasticity and epigenetic marking: An assessment of evidence for genetic accommodation. Evolution 68:656–672CrossRefPubMedGoogle Scholar
- Simo-Riudalbas L, Esteller M (2014) Cancer genomics identifies disrupted epigenetic genes. Hum Genet 133:713–725CrossRefPubMedGoogle Scholar
- Simon JC, Pfrender ME, Tollrian R, Tagu D, Colbourne JK (2011) Genomics of environmentally induced phenotypes in 2 extremely plastic arthropods. J Hered 102:512–525CrossRefPubMedPubMedCentralGoogle Scholar
- Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM (2003) Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 33:70–74CrossRefPubMedGoogle Scholar
- Vickers MH (2014) Early life nutrition, epigenetics and programming of later life disease. Nutrients 6:2165–2178CrossRefPubMedPubMedCentralGoogle Scholar
- Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7:118–126CrossRefGoogle Scholar
- Waddington CH (1956) Genetic assimilation of the bithorax phenotype. Evolution 10:1–13CrossRefGoogle Scholar
- Waddington CH (1957) The strategy of the genes. Allen and Unwin, LondonGoogle Scholar
- Wagner A (2012) The role of robustness in phenotypic adaptation and innovation. Proc Biol Sci 279:1249–1258CrossRefPubMedPubMedCentralGoogle Scholar
- Weiner SA, Toth AL (2012) Epigenetics in social insects: a new direction for understanding the evolution of castes. Genet Res Int 2012:609810. https://doi.org/10.1155/2012/609810 PubMedPubMedCentralGoogle Scholar
- West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
- West-Eberhard MJ (2005a) Developmental plasticity and the origin of species differences. Proc Natl Acad Sci USA 102:6543–6549CrossRefPubMedPubMedCentralGoogle Scholar
- West-Eberhard MJ (2005b) Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B Mol Dev Evol 304:610–618CrossRefPubMedGoogle Scholar