Evolution, the Extended Synthesis

12 - Epigenetic Innovation

12 Epigenetic Innovation Gerd B. Müller The evolution of organismal forms consists of the generation, fixation, and variation of phenotypic characters. The Modern Synthesis concentrated on the last, adaptive variation, essentially avoiding the problem of how complex morphological traits originate and how specific combinations of traits become stabilized as body plans. This variational bias of the Modern Synthesis theory derives from three assumptions necessary for its population genetic formalism to work: (1) all evolution is continuous and gradual; (2) its basis is random and heritable genetic variation; and (3) genetic variation relates directly to phenotypic variation . The resulting abstract scenario accounts for the behavior of gene variation in ideal populations, and natural selection is the sole factor that causes specific phenotypic solutions, which, by the same token, are all adaptive. Therefore, since all its starting points are variational, the Modern Synthesis is confined to explaining, in principle, how existing traits diversify. Despite the concentration of standard evolutionary theory on variation , the problem of innovation has not escaped attention. Darwin (1859), responding to some extent to Mivart’s criticism, had mentioned on several occasions that “characters may have originated from quite secondary causes, independently from natural selection,” and one of the key architects of the Modern Synthesis called innovation “a neglected problem . . . in spite of its importance in a theory of evolution” (Mayr 1960). Schmalhausen, among others (e.g., Rensch 1959), acknowledged the problem of “new differentiations” and suggested considering developmental “tissue reactivity” as its source (Schmalhausen 1949), but the overwhelming success of the population genetic approach during the decades following the Modern Synthesis all but sidelined the issue of innovation. It was more rewarding to calculate the variation of the existing rather than to puzzle over the origination of the unprecedented. 308 Gerd B. Müller During the past few decades, and through the rise of EvoDevo in particular, the situation has changed. Some of the central tenets of the Modern Synthesis have come under scrutiny, and new insights have gained acceptance: phenotypic evolution is not always gradual (Eldredge and Gould 1972; Pagel et al. 2006); not all traits are necessarily adaptive (Gould and Lewontin 1979; Alberch and Gale 1985); and the relationship between genetic variation and the phenotype is far from being simple or direct (Altenberg 2005). Rather, a complex apparatus of developmental transformation intervenes between genotype and phenotype, and the science of EvoDevo has begun to elucidate the evolutionary roles of this apparatus. This has made it possible to begin to address a suite of problems at the phenotype level of evolution that were excluded by the Modern Synthesis approach, such as the origin of structural complexity , biased variation, rapid change of form, and others (Müller and Newman 2005a), the problem of innovation figuring prominently among them. Since the early 1990s a rising number of research papers (overviews in Müller and Newman 2005b; Mozek 2008), books (Nitecki 1990; Margulis and Fester 1991; Schwartz 1999; Müller and Newman 2003; Reid 2007), special issues of journals (Müller and Newman 2005b), and doctoral dissertations (Love 2005) have focused on evolutionary innovation , addressing both empirical and conceptual themes. Several essential questions arise from the treatment of innovation as a special subject in evolutionary theory. Foremost, do phenotypic novelties exist at all, and if so, how are they distinguished from ordinary forms of variation? This is of central importance, because if novelties merely represented a special case of variation,no major consequences for evolutionary theory would ensue. Moreover, if a distinction between phenotypic variation and innovation is possible, are the underlying mechanisms in the realization of innovations also distinct, and what is the role of development in this process? And, finally, does innovation have specific consequences for the patterns and dynamics of organismal evolution? The present chapter explores these questions from an epigenetic perspective (see chapter 7 in this volume for a characterization of the main types of epigenetic research) and summarizes the conceptual contributions of the innovation approach to an extended evolutionary synthesis. The Variation–Innovation Distinction In the standard scheme of evolutionary theory, the problem of phenotypic innovation, if addressed at all, was treated as part of the variation Epigenetic Innovation 309 issue by calling all changes of form “variants,” irrespective of whether or not they were actually based on the variation of a character already present in the primitive condition. Accordingly, morphological novelties were seen as “major variants,” without...