Evolution, the Extended Synthesis

10 - Facilitated Variation

10 Facilitated Variation Marc W. Kirschner and John C. Gerhart Before the rediscovery of Mendel’s laws at the turn of the twentieth century, there was confusion about the source of variation upon which natural selection was thought to act, and about the means by which this variation could be inherited. By the mid-twentieth century much of that confusion had dissipated and a consensus view of evolution, sometimes called the Modern Synthesis, had incorporated population genetics, selection, and chromosomal inheritance into a robust model of evolution . What was still missing were the cellular and molecular mechanisms underlying the generation of the phenotype, particularly the anatomy, physiology, and behavior of multicellular organisms. How relevant such mechanistic understandings were to the theory of evolution was then unclear. Though it is not impossible that molecular discoveries could be both intrinsically fascinating and irrelevant to understanding evolution, we come to the opposite conclusion, that incorporation of these recent cellular and developmental understandings is indispensable for a satisfactory theory of evolution. In our view, evolution as a theory would be incomplete without understanding the nature of phenotypic variation. Such a need was foreshadowed by Sewall Wright, who wrote in 1931: The evolution of complex organisms rests on the attainment of gene combinations which determine a varied repertoire of adaptive cell responses in relation to external conditions. The older writers on evolution were often staggered by the seeming necessity of accounting for the evolution of fine details, for example, the fine structure of all the bones. From the view that structure is never inherited as such, but merely types of adaptive cell behavior which lead to particular types of structure under particular conditions, the difficulty to a considerable extent disappears. (Wright 1931: 147) Although the nature of “adaptive cell behavior” could not have been anticipated by Sewall Wright, recent understandings have shown us a great deal about how cells and organisms produce variation both in 254 Marc W. Kirschner and John C. Gerhart response to the environment and in response to genetic change. The discoveries since the 1970s have revealed a view of the nature of phenotypic variation different from the one assumed by evolutionary biologists in the 1950s and 1960s (Mayr 1963). As we shall argue, these new understandings require a reappraisal of the contention that natural selection is the sole creative force in evolution. Novelty arises from an interplay between the properties of the organism and mutation under selection. The nature of the developmental and cellular circuits contributes a great deal to the kinds of variation that selection can act upon. We have summarized these ideas recently,in a theory of facilitated variation (Kirschner and Gerhart 2005, Gerhart and Kirschner, 2007). We shall explore both the origins of the new understandings and the understandings themselves , and their implications for evolutionary theory. The Problem of Phenotypic Variation Variation is indispensable to evolution: individuals in a population of organisms inevitably vary slightly in phenotype. Some of these variations are heritable. In the environmental conditions met by the population, some variant individuals reproduce better than others, due to their heritable phenotypic difference. They are selected, and their offspring carry the genetic, and hence the phenotypic, difference. In the broad view of evolution, all living organisms are related by descent from a first ancestor , and over the eons have diverged to diverse forms and adaptive functions by the gradual accumulation of selected phenotypic variations. This picture of evolution is widely accepted; most of these propositions go back to Darwin himself. The most important addition, contributed by the Modern Synthesis in the mid-twentieth century, was the insight that heritable phenotypic change requires genetic change, and that genetic change is random with respect to targets and the environment. Selection was established as central, and genetic change was established as the underlying cause of heritable variation. Today, genetic change is well understood in light of our knowledge of DNA structure, replication, rearrangements, damage and repair, and the comparison of genome sequences. Genetic variation is interesting because it is at the start of the causal chain to new phenotypes, because it is random, because it is easily tracked by mating experiments and sequencing, and because it is easily expressible in mathematical terms. Understanding that genetic change generates phenotypic change, and that the latter is selected upon, favorably or unfavorably, gives a self- Facilitated Variation 255 consistent and satisfying picture of evolution. Since the selected phenotype always carries...