Abstract
In responding to three reviews of Evolution in Four Dimensions (Jablonka and Lamb, 2005, MIT Press), we briefly consider the historical background to the present genecentred view of evolution, especially the way in which Weismann’s theories have influenced it, and discuss the origins of the notion of epigenetic inheritance. We reaffirm our belief that all types of hereditary information—genetic, epigenetic, behavioural and cultural—have contributed to evolutionary change, and outline recent evidence, mainly from epigenetic studies, that suggests that non-DNA heritable variations are not rare and can be quite stable. We describe ways in which such variations may have influenced evolution. The approach we take leads to broader definitions of terms such as ‘units of heredity’, ‘units of evolution’, and ‘units of selection’, and we maintain that ‘information’ can be a useful concept if it is defined in terms of its effects on the receiver. Although we agree that evolutionary theory is not undergoing a Kuhnian revolution, the incorporation of new data and ideas about hereditary variation, and about the role of development in generating it, is leading to a version of Darwinism that is very different from the gene-centred one that dominated evolutionary thinking in the second half of the twentieth century.
Similar content being viewed by others
References
Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654
Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469
Avital E, Jablonka E (2000) Animal traditions: behavioural inheritance in evolution. Cambridge University Press, Cambridge
Bateman RM, DiMichele WA (2002) Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor and Francis, London, pp 109–159
Bennett-Baker PE, Wilkowski J, Burke DT (2003) Age-associated activation of epigenetically repressed genes in the mouse. Genetics 165:2055–2062
Chong S, Whitelaw E (2004) Epigenetic germline inheritance. Curr Opin Genet Develop 14:692–696
Cronk QCB (2001) Plant evolution and development in a post-genomic context. Nat Rev Genet 2:607–619
De Vries H (1906) The origin of the peloric toad-flax. Chapter 16 of Species and varieties, their origin by mutation. 2nd edn. Open Court, Chicago, pp 459–487
Drake JW, Charlesworth B, Charlesworth D, Crow JF (1998) Rates of spontaneous mutation. Genetics 148:1667–1686
Fragaszy DM, Perry S (2003) The biology of traditions: models and evidence. Cambridge University Press, Cambridge
Garcia-Fernàndez J (2005) The genesis and evolution of homeobox gene clusters, Nat Rev Genet 6:881–892
Gluckman P, Hansen M (2005) The fetal matrix: Evolution, development and disease. Cambridge University Press, Cambridge
Grant-Downton RT, Dickinson HG (2005) Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Annl Bot 96:1143–1164
Grant-Downton RT, Dickinson HG (2006) Epigenetics and its implications for plant biology. 2. The ‘epigenetic epiphany’: epigenetics, evolution and beyond. Annl Bot 97:11–27
Griesemer JR (2002) What is “epi” about epigenetics? Annl NY Acad Sci 981:97–110
Griesemer JR, Wimsatt WC (1989) Picturing Weismannism: a case study of conceptual evolution. In: Ruse M (ed) What the philosophy of biology is: essays dedicated to David Hull. Kluwer, Dordrecht, pp 75–137
Haig D (2004) The (dual) origin of epigenetics. Cold Spring Harbor Symp Quantitative Biol 69:67–70
Holliday R (1987) The inheritance of epigenetic defects. Science 238:163–170
Holliday R (2006) Epigenetics: a historical overview. Epigenetics 1:76–80
Jablonka E (2002) Information: its interpretation, its inheritance, and its sharing. Philos Sci 69:578–605
Jablonka E (2004) From replicators to heritably varying phenotypic traits: the extended phenotype revisited. Biol Philos 19:353–375
Jablonka E, Lamb MJ (1995) Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford University Press, Oxford
Jablonka E, Lamb MJ (2002) The changing concept of epigenetics. Annl NY Acad Sci 981:82–96
Jablonka E, Lamb MJ (2006) The evolution of information in the major transitions. J Theoret Biol 239:236–246
Johannsen W (1911) The genotype conception of heredity. Am Nat 45:129–159
Kidwell MG, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94:7704–7711
Lachmann M, Jablonka E (1996) The inheritance of phenotypes: an adaptation to fluctuating environments. J Theoret Biol 181:1–9
Levy AA, Feldman M (2004) Genetic and epigenetic reprogramming of the wheat genome upon allopolyploidization. Biol J Linnean Soc 82:607–613
Lolle SJ, Victor JL, Young JM, Pruitt RE (2005) Genome-wide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434:505–509
Maynard Smith J (2000) The concept of information in biology. Philos Sci 67:177–194
Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. Freeman, Oxford
Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annl Rev Neurosci 24:1161–1192
Nanney DL (1958) Epigenetic control systems. Proc Natl Acad Sci USA 44:712–717
Oyama S (1985) The ontogeny of information: developmental systems and evolution. Cambridge University Press, Cambridge
Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91
Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441:469–474
Richards EJ (2006) Inherited epigenetic variation—revisiting soft inheritance. Nat Rev Genet 7:395–401
Richerson PJ, Boyd R (2005) Not by genes alone: how culture transformed human evolution. University of Chicago Press, Chicago
Roberts BT, Wickner RB (2003) Heritable activity: a prion that propagates by covalent autoactivation. Genes Develop 17:2083–2087
Rodin SN, Parkhomchuk DV, Riggs AD (2005) Epigenetic changes and repositioning determine the evolutionary fate of duplicated genes. Biochemistry (Moscow) 70:559–567
Romanes GJ (1888) Lamarckism versus Darwinism. Nature 38:413
Romanes GJ (1893) An examination of Weismannism. Longmans, Green, & Co., London
Rudall PJ, Bateman RM (2003) Evolutionary change in flowers and inflorescences: evidence from naturally occurring terata. Trends Plant Sci 8:76–82
Simpson GG (1949) The meaning of evolution. Yale University Press, Newhaven
Simpson GG (1960) The world into which Darwin led us. Science 131:966–974
Stam M, Mittelsten-Scheid O (2005) Paramutation: an encounter leaving a lasting impression. Trends Plant Sci 10:283–290
Takeda S, Paszkowski J (2006) DNA methylation and epigenetic inheritance during plant gametogenesis. Chromosoma 115:27–35
Vrana PB, Fossella JA, Matteson P, del Rio T, O’Neill MJ, Tilghman SM (2000) Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus. Nat Genet 25:120–124
Waddington CH (1957) The strategy of the genes. Allen & Unwin, London
Waddington CH (1975) The evolutionist of an evolutionist. Edinburgh University Press, Edinburgh
Weaver ICG, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847–854
Weismann A (1893). The Germ-plasm: a theory of heredity (trans. by Parker W.N. and Rönnfeldt H.). Walter Scott, London
Weismann A (1902) On germinal selection as a source of definite variation, 2nd edn (trans. McCormack T.J.). Open Court, Chicago
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
Wickner RB, Edskes HK, Ross ED, Pierce MM, Baxa U, Brachmann A, Shewmaker F (2004) Prion genetics: new rules for a new kind of gene. Annl Rev Genet 38:681–707
Wilson EB (1900) The cell in development and inheritance. Macmillan, New York
Winther RG (2001) August Weismann on germ-plasm variation. J History Biol 34:517–555
Zilberman D, Henikoff S (2005) Epigenetic inheritance in Arabidopsis: selective silence. Curr Opin Genet Develop 15:557–562
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jablonka, E., Lamb, M.J. The expanded evolutionary synthesis—a response to Godfrey-Smith, Haig, and West-Eberhard. Biol Philos 22, 453–472 (2007). https://doi.org/10.1007/s10539-007-9064-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10539-007-9064-z