Epigenetics: ambiguities and implications

Abstract

Everyone has heard of ‘epigenetics’, but the term means different things to different researchers. Four important contemporary meanings are outlined in this paper. Epigenetics in its various senses has implications for development, heredity, and evolution, and also for medicine. Concerning development, it cements the vision of a reactive genome strongly coupled to its environment. Concerning heredity, both narrowly epigenetic and broader ‘exogenetic’ systems of inheritance play important roles in the construction of phenotypes. A thoroughly epigenetic model of development and evolution was Waddington’s aim when he introduced the term ‘epigenetics’ in the 1940s, but it has taken the modern development of molecular epigenetics to realize this aim. In the final sections of the paper we briefly outline some further implications of epigenetics for medicine and for the nature/nurture debate.

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Notes

  1. 1.

    We owe this point to one of the anonymous reviewers.

  2. 2.

    Jablonka and Lamb’s identification of epigenetic inheritance with the ‘Lamarckian’ inheritance of acquired characters is not unproblematic. Some scientists insist that the term Lamarckian inheritance should be restricted to the inheritance of phenotypic (somatic) characters that are acquired during development (Hall 2011, p. 11).

  3. 3.

    Even non-heritable epigenetic variation can have an impact on evolution. Through its role in gene expression, this variation differentially changes the survival and reproduction of an individual organism and therefore enables other factors to be transmitted, which thanks to the epigenetic variant can therefore spread in the population (we owe this point to a comment by one of the reviewers).

References

  1. Amundson, R. (2005). The changing role of the embryo in evolutionary thought: roots of evo-devo. In Michael Ruse (Ed.), Cambridge studies in philosophy and biology. Cambridge: Cambridge University Press.

    Google Scholar 

  2. Badyaev, A. V., & Uller, T. (2009). Parental effects in ecology and evolution: mechanisms, processes, and implications. Philosophical Transactions of the Royal Society, Biological Sciences, 364, 1169–1177.

    Article  Google Scholar 

  3. Badyaev, A. V. (2009). Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philosophical Transactions of the Royal Society B, 364, 1125–1141.

    Article  Google Scholar 

  4. Bateson, P., Barker, P., Clutton-Brock, T., Deb, D., D’Udine, B., Foley, R. A., et al. (2004). Developmental plasticity and human health. Nature, 430, 419–421.

    Article  Google Scholar 

  5. Bateson, P., & Gluckman, P. D. (2011). Plasticity, robustness, development and evolution. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  6. Bateson, P., & Martin, P. (1999). Design for a life: How behavior and personality develop. London: Jonathan Cape.

    Google Scholar 

  7. Bell, C. G., & Beck, S. (2010). The epigenomic interface between genome and environment in common complex diseases. Brief Functional Genomics, 9(5–6), 477–485.

    Article  Google Scholar 

  8. Bergstrom, C., & Rosvall, M. (2009). The transmission sense of information. Biology and Philosophy, 26(2), 159–176.

    Article  Google Scholar 

  9. Bonasio, R., Tu, S., & Reinberg, D. (2010). Molcecular signals of epigenetic states. Science, 330(6004), 612–616.

    Article  Google Scholar 

  10. Bonduriansky, R. (2012). Rethinking heredity, again. Tree, 27(6), 330–336.

    Google Scholar 

  11. Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868–873.

    Article  Google Scholar 

  12. Burian, R. M. (2004). Molecular epigenesis, molecular pleiotropy, and molecular gene definitions”. History and Philosophy of the Life Sciences, 26(1), 59–80.

    Article  Google Scholar 

  13. Champagne, F. A., & Curley, J. P. (2009). Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neuroscience and Biobehavioral Reviews, 33(4), 593–600.

    Article  Google Scholar 

  14. Crick, F. H. C. (1958). On protein synthesis. Symposia of the Society for Experimental Biology, 12, 138–163.

    Google Scholar 

  15. Danchin, É., Charmantier, A., Champagne, F. A., Mesoudi, A., Pujol, B., & Blanchet, S. (2011). Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution. Nature Reviews Genetics, 12(7), 475–486.

    Article  Google Scholar 

  16. Davidson, N. O. (2002). The challenge of target sequence specificity in C→U RNA editing. The Journal of Clinical Investigation, 109(3), 291–294.

    Article  Google Scholar 

  17. Gilbert, S. F., & Epel, D. (2009). Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sunderland: Sinauer Associates.

    Google Scholar 

  18. Gilbert, S. F. (2001). Ecological developmental biology: developmental biology meets the real world. Developmental Biology, 233, 1–22.

    Article  Google Scholar 

  19. Gluckman, P. D., Hanson, M. A., Bateson, P., Beedle, A. S., Law, C. M., Bhutta, Z. A., et al. (2009). Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet, 373(9675), 1654–1657.

    Article  Google Scholar 

  20. Gluckman, P. D., & Hanson, M. A. (2005a). The fetal matrix: evolution, development and disease. Cambridge: Cambridge University Press.

    Google Scholar 

  21. Gluckman, P. D., & Hanson, M. A. (Eds.). (2005b). Developmental origin of health and disease. Cambridge: Cambridge University Press.

    Google Scholar 

  22. Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007). Non-genomic transgenerational inheritance of disease risk. BioAssays, 29(2), 145–154.

    Article  Google Scholar 

  23. Gluckman, P. D., Hanson, M. A., & Spencer, H. G. (2005). Predictive adaptive responses and human evolution. Trends in Ecology & Evolution, 20(10), 527–533.

    Article  Google Scholar 

  24. Godfrey, K. M., Sheppard, A., Gluckman, P. D., Lillycrop, K. A., Burdge, G. C., McLean, C., et al. (2011). Epigenetic gene promoter methylation at birth is associated with child’s later adiposity. Diabetes, 30(5), 1528–1534.

    Article  Google Scholar 

  25. Godfrey-Smith, P. (2000). On the theoretical role of “genetic coding”. Philosophy of Science, 67(1), 26–44.

    Article  Google Scholar 

  26. Gottlieb, G. (1992). Individual development and evolution. Oxford: Oxford University Press.

    Google Scholar 

  27. Gottlieb, G. (1997). Synthesizing nature-nurture: Prenatal roots of instinctive behavior. Hillsdale: Lawrence Erlbaum Assoc.

    Google Scholar 

  28. Griffiths, P. E. (2003). Beyond the baldwin effect: James Mark Baldwin’s ‘social heredity’, epigenetic inheritance and niche-construction. In Bruce H. Weber & David J. Depew (Eds.), Evolution and learning: The baldwin effect reconsidered (pp. 193–215). Cambridge: MIT Press.

    Google Scholar 

  29. Griffiths, P. E., & Tabery, J. T. (2013). Developmental systems theory: what does it explain, and how does it explain it? In R. M. Lerner & J. B. Benson (Eds.), Embodiment and epigenesis: Theoretical and methodological issues in understanding the role of biology within the relational developmental system part a: philosophical, theoretical, and biological dimensions (pp. 65–94). Amsterdam: Elsevier.

    Google Scholar 

  30. Griffiths, P. E., & Stotz, K. (2013). Genetics and philosophy: An introduction. In Michael Ruse (Ed.), Cambridge introductions to philosophy and biology. Cambridge: Cambridge University Press.

    Google Scholar 

  31. Griffiths, P. E., Pocheville, A., Calcott, B., Stotz, K., Kim, H., & Knight, R. (2015). Measuring causal specificity. Philosophy of Science, 82(4), 529–555.

    Article  Google Scholar 

  32. Haig, D. (2000). The kinship theory of genomic imprinting. Annual Review of Ecology and Systematics, 31, 9–32.

    Article  Google Scholar 

  33. Haig, D. (2004). The (dual) origin of epigenetics. Cold Spring Harbor Symposia on Quantitative Biology, 69, 67–70.

    Article  Google Scholar 

  34. Hall, B. K. (2011). A brief history of the term and concept of epigenetics. In B. Hallgrimsson & B. K. Hall (Eds.), Epigenetics: Linking genotype and phenotype in develoment and evolution (pp. 9–13). Berkeley: University of California Press.

    Google Scholar 

  35. Hallgrimsson, B., & Hall, B. K. (2011). Introduction. In B. Hallgrimsson & B. K. Hall (Eds.), Epigenetics: Linking genotype and phenotype in develoment and evolution (pp. 1–5). Berkeley: University of California Press.

    Google Scholar 

  36. Herring, S. W. (1993). Formation of the vertebrate face: epigenetic and functional influences. American Zoologist, 33(4), 472–483.

    Article  Google Scholar 

  37. Holliday, R. (1987). The inheritance of epigenetic defects. Science, 238(4824), 163–170.

    Article  Google Scholar 

  38. Holliday, R. (1994). Introduction: epigenetics, an overview. Developmental Genetics, 15, 453–457.

    Article  Google Scholar 

  39. Holliday, R. (2006). Epigenetics: A historical overview. Epigenetics, 1(2), 76–80.

    Article  Google Scholar 

  40. Jablonka, E. (2001). The systems of inheritance. In Susan Oyama, Paul E. Griffiths, & Russell D. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 99–116). Cambridge: MIT Press.

    Google Scholar 

  41. Jablonka, E., & Avital, E. (2001). Animal traditions: Behavioural inheritance in evolution. Cambridge: Cambridge University Press.

    Google Scholar 

  42. Jablonka, E., & Lamb, M. J. (1995). Epigenetic inheritance and evolution: The lamarkian dimension. Oxford: Oxford University Press.

    Google Scholar 

  43. Jablonka, E., & Lamb, M. J. (2005). Evolution in four dimensions: Genetic, epigenetic, behavioral, and symbolic variation in the history of life. Cambridge: The MIT Press.

    Google Scholar 

  44. Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol, 84(2), 131–176.

    Article  Google Scholar 

  45. Jirtle, R. L., & Skinner, M. K. (2007). Environmental epigenomics and disease susceptibility. Nature Reviews Genetics, 8, 253–262.

    Article  Google Scholar 

  46. Kronfeldner, M. (2016a). The authority of nature and why we disagree about human nature. In T. Lewens & B. Hannon (Eds.), Why we disagree about human nature. Oxford: Oxford University Press.

    Google Scholar 

  47. Kronfeldner, M. (2016b). The right to ignore: An epistemic defense of the nature/culture divide. In R. Joyce (Ed.), Commissioned for the Routledge handbook of evolution and philosophy. London: Routledge.

    Google Scholar 

  48. Lamm, E., & Jablonka, E. (2008). The nurture of nature: hereditary plasticity in evolution. Philosophical Psychology, 21(3), 305–319.

    Article  Google Scholar 

  49. Lande, R., & Price, T. (1989). Genetic correlations and maternal effect coefficients obtained from offspring-parent regression. Genetics, 122(4), 915–922.

    Google Scholar 

  50. Meaney, M. J. (2001a). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review Neuroscience, 24, 1161–1192.

    Article  Google Scholar 

  51. Meaney, M. J. (2001b). Nature, nurture, and the disunity of knowledge. Annals New York Academy of Sciences, 935, 50–61.

    Article  Google Scholar 

  52. Meaney, M. J., & Szyf, M. (2005). Environmental programming of stress responses through DNA methylation: Life at the interface between a dynamic environment and a fixed genome. Dialogues in Clinical Neuroscience, 7(2), 103–123.

    Google Scholar 

  53. Morgan, T. H., Sturtevant, A. H., Muller, H. J., & Bridges, C. B. (1915). The mechanism of mendelian heredity. New York: Henry Holt.

    Book  Google Scholar 

  54. Nanney, D. L. (1958). Epigenetic control systems. Proceedings of National Academy of Sciences, 44, 712.

    Article  Google Scholar 

  55. Nanney, D. L. (1959). Epigenetic factors affecting mating type expression in certain ciliates. Cold Spring Harbor symposia on quantitative biology, 23, 327.

    Article  Google Scholar 

  56. Noble, D. (2015). Conrad Waddington and the origin of epigenetics. Journal of Experimental Biology, 218, 816–818.

    Article  Google Scholar 

  57. O’Malley, M. A., & Stotz, K. (2011). Intervention, integration and translation in obesity research: genetic, developmental and metaorganismal approaches. Philosophy, Ethics, and Humanities in Medicine,. doi:10.1186/1747-5341-6-2.

    Google Scholar 

  58. Oyama, S. (1985). The ontogeny of information: Developmental systems and evolution. Cambridge: Cambridge University Press.

    Google Scholar 

  59. Oyama, S. (2002). The nurturing of natures. In A. Grunwald, M. Gutmann & E. M. Neumann-Held (Eds.), On human nature: Anthropological, biological and philosophical foundations (pp. 163–170). Berlin: Springer.

  60. Petronis, A. (2010). Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature, 465, 721–727.

    Article  Google Scholar 

  61. Pigliucci, M. (2001). Phenotypic plasticity: beyond nature and nurture, syntheses in ecology and evolution. Baltimore: The Johns Hopkins University Press.

    Google Scholar 

  62. Ptashne, M., & Gann, A. (2002). Genes and signals. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  63. Sarkar, S. (1996). Biological information: A sceptical look at some central dogmas of molecular biology. In S. Sarkar (Ed.), The Philosophy and history of molecular biology: New perspectives (pp. 187–232). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  64. Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland: Sinauer.

    Google Scholar 

  65. Schmalhausen, I. I. (1949). Factors of evolution: The theory of stabilising selection. translated by I Dordick. Philadelphia and Toronto: Blakeston.

    Google Scholar 

  66. Stotz, K. (2006a). With genes like that, who needs an environment? Postgenomics’ argument for the ontogeny of information. Philosophy of Science, 73(5), 905–917.

    Article  Google Scholar 

  67. Stotz, K. (2006b). Molecular epigenesis: distributed specificity as a break in the Central Dogma’. History and Philosophy of the Life Sciences, 28(4), 527–544.

    Google Scholar 

  68. Sultan, S. E. (2007). Development in context: the timely emergence of eco-devo. Trends in Ecology & Evolution, 22(11), 575–582.

    Article  Google Scholar 

  69. Suzuki, Y., & Nijhout, H. F. (2006). Evolution of a polyphenism by genetic accommodation. Science, 311(5761), 650–652.

    Article  Google Scholar 

  70. Uller, T. (2012). Parental effects in development and evolution. In Nick J. Royle, Per T. Smiseth, & Mathias Kölliker (Eds.), The evolution of parental care. Oxford: Oxford University Press.

    Google Scholar 

  71. Waddington, C. H. (1940). Organisers and genes. Cambridge: Cambridge University Press.

    Google Scholar 

  72. Waddington, C. H. (1952). The evolution of developmental systems. In D. A. Herbert (Ed.), Twenty-eighth meeting of the Australian and New Zealand association for the advancement of science. Brisbane: A.H Tucker, Government Printer Brisbane.

    Google Scholar 

  73. Waddington, C. H. (1953a). Genetic assimilation of an acquired character. Evolution, 7, 118–126.

    Article  Google Scholar 

  74. Waddington, C. H. (1953b). The “Baldin Effect”, “Genetic Assimilation” and “Homeostasis”. Evolution, 7(4), 386–387.

    Google Scholar 

  75. Wade, M. J. (1998). The evolutionary genetics of maternal effects. In T. A. Mousseau & C. W. Fox (Eds.), Maternal effects as adaptations (pp. 5–21). Oxford: Oxford University Press.

    Google Scholar 

  76. Weaver, I. C. G., Cervoni, N., Champagne, F. A., D’Alessio, A. C., Sharma, S., Seckl, J. P., et al. (2004a). Epigenetic programming by maternal behavior. Nature Neuroscience, 7(8), 847–854.

    Article  Google Scholar 

  77. Weaver, I. C. G., Diorio, J., Seckl, J. R., Szyf, M., & Meaney, M. J. (2004b). Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Annals of the New York Academy of Sciences, 1024, 182–212.

    Article  Google Scholar 

  78. Weber, B. H., & Depew, D. J. (Eds.). (2003). Evolution and learning: The Baldwin effect reconsidered. Cambridge: MIT Press.

    Google Scholar 

  79. West, M. J., & King, A. P. (1987). Settling nature and nurture into an ontogenetic niche. Developmental Psychobiology, 20(5), 549–562.

  80. West, M. J., King, A. P., & White, D. J. (2003). The case for developmental ecology. Animal Behaviour, 66, 617–622.

    Article  Google Scholar 

  81. West-Eberhard, M. J. (1998). Evolution in the light of developmental and cell biology, and vice versa. PNAS, 95, 8417–8419.

    Article  Google Scholar 

  82. West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.

    Google Scholar 

  83. West-Eberhard, M. J. (2005a). Phenotypic accommodation: Adaptive innovation due to developmental plasticity. Journal of Experimental Zoology Part B, 304B, 610–618.

    Article  Google Scholar 

  84. West-Eberhard, M. J. (2005b). Developmental plasticity and the origin of species differences. PNAS, 102(Suppl 1), 6543–6549.

    Article  Google Scholar 

  85. Wilkins, A. (2011). Epigenetic inheritance: Where does the field stand today? What do we still need to know? In S. B. Gissis & E. Jablonka (Eds.), Transformations of lamarckism: From subtle fluids to molecular biology (pp. 389–393). Cambridge: The MIT Press.

    Google Scholar 

  86. Wolff, G. L., Kodell, R. L., Moore, S. R., & Cooney, C. A. (1998). Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J, 12, 949–957.

    Google Scholar 

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Funding

This project/publication was made possible through the support of a grant from the Templeton World Charity Foundation: Causal Foundations of Biological Information TWCF0063/AB37. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the Templeton World Charity Foundation.

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Correspondence to Karola Stotz.

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This article is part of the topical collection "Sketches of a conceptual history of epigenesis".

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Stotz, K., Griffiths, P. Epigenetics: ambiguities and implications. HPLS 38, 22 (2016). https://doi.org/10.1007/s40656-016-0121-2

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Keywords

  • Epigenetics
  • Epigenesis
  • Epigenetic inheritance
  • Exogenetic inheritance
  • Genetic assimilation
  • Genetic accommodation