Evolution, the Extended Synthesis

7 - Transgenerational Epigenetic Inheritance

7 Transgenerational Epigenetic Inheritance Eva Jablonka and Marion J. Lamb Since the 1990s, a growing number of evolution-oriented biologists have expressed the view that the foundations of the Modern Synthesis—the evolutionary paradigm that was constructed during the 1930s and 1940s and has dominated views of evolution for the past 60 years—need rethinking. They believe that the construction of a new, extended, evolutionary synthesis is under way. Challenges to the Modern Synthesis view have been coming from many directions, most notably from developmental biology, microbiology, ecology, animal behavior, and cultural studies. In this chapter we focus mainly on developmental biology, in particular on molecular studies of epigenetics, and on one specific challenge : the challenge of “soft inheritance.” Soft inheritance occurs when new variations that are the result of environmental effects are transmitted to the next generation (Mayr 1982). In order to understand the nature of this challenge, we first summarize the assumptions about heredity and development that were built into the late twentieth-century version of the Modern Synthesis. This synthesis defined itself not only by what it included, but also by what it explicitly excluded or marginalized .We emphasize these excluded and marginalized issues because they are among those that are being most strongly contested today. The late twentieth-century version of the Modern Synthesis assumed: 1. Heredity occurs through the transmission of germ-line genes. Genes are discrete units of DNA that are located in chromosomes. Hereditary variations are the result of differences in DNA base sequence. There are no inherited variations that cannot be expressed in terms of inherited genetic differences. 2. Hereditary variation is the consequence of (1) the many random combinations of preexisting alleles that are generated by the sexual processes; and (2) new variations (mutations) resulting from accidental 138 Eva Jablonka and Marion J. Lamb changes in DNA. Hereditary variation is not affected by the developmental history of the individual. There is no “soft inheritance.” 3. Heritable variations usually have small effects, and evolution is typically gradual. Through the selection of individuals with phenotypes that make them slightly more adapted to their environment than are other individuals in the population,some alleles increase in frequency.Mutation pressure is not an important factor in evolution. With a few exceptions, macroevolution is continuous with microevolution, and does not require any additional processes. 4. The ultimate unit of selection is the gene. Although genes interact and the interactions are often nonlinear, the additive fitness effects of single genes (which can be extracted from the fitness effects of the developmental networks in which they participate) drive evolution by natural selection. The genetic-developmental network and the phenotype it generates are not heritable and cannot be a unit of evolution. 5. Morphological innovations, like all innovations, are the results of gene mutations that, when beneficial, accumulate over time and lead to a qualitatively new form. Generic, physical-chemical properties of biological matter, which underlie plasticity, have no role in morphological and physiological innovations other than specifying the boundaries of the forms that are possible. 6. The targets of selection are individuals, which are well-defined entities. Although conspecifics in groups interact and may co-evolve with each other as well as with their symbionts and parasites, group selection and community selection are rare. Species selection may exist, but is of marginal significance. The community is only rarely a target of selection, and species selection cannot explain the main patterns of macroevolution. 7. Evolution occurs through modifications from a common ancestor, and is based on vertical descent. Horizontal transfer of genes or other types of information has only minor significance, and does not alter the basic branching structure of phylogenies. The main pattern of evolutionary divergence is, at all times and for all taxa, treelike, not weblike. Biologists are now questioning each of these assumptions, arguing that: 1. Heredity involves more than DNA. There are heritable variations that are independent of variations in DNA sequence, and they have a Transgenerational Epigenetic Inheritance 139 degree of autonomy from DNA variations. These non-DNA variations can form an additional substrate for evolutionary change, and also guide genetic evolution (Jablonka and Lamb 1995, 2005; Jablonka and Raz 2009). 2. Soft inheritance, the inheritance of developmentally induced and regulated variations, exists, and is likely to be important. It involves both non-DNA variations and developmentally induced variations in DNA sequences (Jablonka and...