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9 Epigenetics: Linking Genotype and Phenotype in Development and Evolution, ed. Benedikt Hallgrímsson and Brian K. Hall. Copyright © by The Regents of the University of California. All rights of reproduction in any form reserved. 2 A Brief History of the Term and concept Epigenetics Brian K. Hall conTenTs Epigenesis or Preformation Nucleus or Cytoplasm Epigenetics: An Integrated Approach Epigenetic Inheritance References This chapter provides a brief evaluation of the history of epigenetics as a term and as a concept . Although the term was not coined until the 1940s, the concept that genes are influenced by factors beyond the genome (the “epi” in epigenetics) is much older and can be traced to late nineteenth-century discussions of whether the nucleus or the cytoplasm “controlled” development , to earlier nineteenth-century discussions of whether the sperm or egg provided the primary material for development and therefore for life, and even earlier to the eighteenthcentury concepts of organismal structure as either preformed and arising by unfolding—the original use of the term evolution—or arising gradually by epigenesis. ePIgenesIs oR PRefoRmATIon Two parallel approaches to how organisms arise can be traced back to the 4th century BCE and the writings of the Greek philosopher Aristotle (384–322 BCE). Developed specifically to explain animal embryogenesis (development), the concepts have become known as preformation— the gradual unfolding through growth of features preformed in the egg or sperm—and epigenesis—the successive differentiation of features during development leading to increasing complexity and the formation of the adult form. Charles Bonnet (1720–1793) enshrined preformation in the eighteenth century with his embo îtment, or encapsulation, theory, in which all the members of all future generations were present in an early developmental stage: cotyledons within the seeds of plants, future generations of insects in the pupa. The ability of Hydra to regenerate the entire body or of newts to regenerate their tails was interpreted as the unfolding of preformed features (Farley, 1982; Dinsmore, 1991; Hall, 1998b). 10 historical and philosophical foundations The term epigenesis may have first been used by the German anatomist and embryologist Caspar Friedrich Wolff (1733–1794), whose dissections of chicken embryos revealed the progressive development of the tubular gut and led him to conclude that “When the formation of the intestine in this manner has been duly weighed, almost no doubt can remain, I believe, of the truth of epigenesis” (Wolff, 1768–1769, 460–61). Wolff also proposed a series of causal links between developing parts of the embryo: “each part is first of all an effect of the preceding part, and itself becomes the cause of the following part” (Wolff, 1764, 211). Preformation lost further support in the early 1800s with the publication of the investigations of chicken embryological development by Louis Sébastien Tredern and Christian Pander and the even more extensive studies by the comparative embryologist Karl von Baer (1792–1876), who demonstrated that vertebrate embryos differentiate from a foundation of fundamental germ layers (primary differentiation), followed by histological and then morphological differentiation (Hall, 1997; Horder, 2008). nucleus oR cyToPlAsm The transition from preformation to epigenesis ruled out gradual unfolding as the basis for development but provided neither a proximate mechanism for how embryos develop nor an ultimate mechanism for how the same type of embryo appears generation after generation when individuals from a single species are bred. Part of the resolution is that some preformed features are passed on from generation to generation , including the cytoplasmic constituents of the egg, mitochondrial DNA, and the nuclear genetic constituents from the combined contributions of the male and female parents. Indeed, much of the latter part of the nineteenth century and the first decades of the twentieth were taken up with endeavors to determine whether cytoplasm or nucleus “controlled” embryonic development and so controlled life (Wilson, 1925; see Hall, 1983, 1998a, 1998b; and the papers in Laubichler and Maienschein, 2007, for evaluations). The leading cell biologist of the early twentieth century, E.B. Wilson (1856–1939), equated preformation and epigenesis with nuclear or cytoplasmic control. On the basis of extensive and exhaustive analyses of cell lineages in invertebrate embryos, Wilson assigned determination to the nucleus and an initiating role to the cytoplasm: Fundamentally, however, we reach the conclusion that in respect to a great number of characters heredity is effected by the transmission of a nuclear preformation which in the course of development finds expression in a process of cytoplasmic epigenesis. (Wilson, 1925, 1112; emphasis in original) EpigEnEtics • An Integrated Approach The definition...

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