EVOLUTION AND BIFURCATION OF DEVELOPMENTAL PROGRAMS

The idea that development can tell us something about the organization of the diversity of life predates the establishment of Darwinian evolution. For example, Agassiz (1849) presented a very elaborate theory illustrating the parallelism between the hierarchical organization of life (immutable and a reflection of God's plan) and the sequential process of ontogeny. With the advent of Darwinian evolution and Haeckel's "biogenetic law," embryology became a major source of evidence for evolutionary transformation. Embryology and evolution were intimately related disciplines; indeed, Darwin remarked that "Embryology is to me by far the strongest single class of facts in favor of change of forms" (letter of Darwin to Asa Gray quoted in Gould, 1977 p. 70). However, the situation drastically changed around the early 1930s with the advent of experimental embryology on one hand and the preponderance of population genetics in evolutionary studies on the other. Today, despite its recognized significance, the role of morphogenetic interactions in controlling phyletic transformations remains to be successfully integrated into the body of evolutionary theory. Although numerous pleas in favor of the crucial significance of development in evolutionary biology have been made (cf. Devillers, 1965; Maderson, 1975; Horder, 1981; Rachootin and Thomson, 1981, among many others), modern textbooks on evolution make only scant reference to developmental biology (see Dobzhansky et al., 1977, for a recent example). Recently, Alberch (1980) addressed the role of epigenetic interactions in constraining the patterns of variation in phylogeny. Various lines of evidence led him to the following conclusions about the apportionment of morphological variation in phenotype space (cf. Fig. 1): (1) Phenotypes are discrete. That is, points are not distributed uniformly over phenotype space, but tend to cluster around major "themes," corresponding to taxa or classes of teratologies. (2) While there may be considerable dispersion around a morphological theme, the variability in any trait is definitely limited. (3) When new morphological themes arise, either in ontogeny or phylogeny, the transitions between themes are not random. (4) These properties are largely a result of epigenetic interactions during development. Here we shall re-examine these generalizations from a mechanistic viewpoint, asking the question: how can developmental processes, at the cell and tissue level, control the expression of morphological variation and generate the rules of phenotypic transformation during phyletic evolution? It is a truism that any change in morphology is necessarily produced by a change in developmental processes, and consequently we agree with Waddington (1975) that morphological evolution can be defined as the change in developmental programs during phylogeny. However, in order to render such a view operational we must state unambiguously what we mean by a "developmental program. " This is the main objective of this paper (see also Alberch, 1981, for additional discussion on the structure and nature of this concept). We remark that the true "developmental program" has perhaps a more deterministic connotation than we intend here. Embryogenesis may appear quite deterministic on a macroscopic scale; however, at the cellular level events pro-