Evolutionary Novelty and Innovation

It has often been argued that the differences in morphology seen in the Cambrian explosion seem more 'fundamental' than the differences in body shape and color seen in recent adaptive radiations because of a retrospective fallacy, that is, we define certain characters as more fundamental simply because they are older. While this may be true for certain characters (e.g., traits that define higher taxa in some groups vary intraspecifi-cally in others), it is hard to escape from the view that the presence or absence of a coelom, body segments, and limbs reflect greater and more fundamental differences in genetics, development, and ecology than the shape of a finch's beak or a cichlid's teeth. Therefore, evolutionists are left with the very real question of why certain periods in the history of life are characterized by major novelties in morphology and modes of life.

It was because of this question that macromutationism and Goldschmidt's ''hopeful monsters'' had such appeal. The theoretical edifice of Neo-Darwinism, population and quantitative genetics, assumed a fixed space defined by preexisting quantitative traits and loci. The theory of mutation, selection, and genetic drift described the dynamics of populations in this space, but had little to say about how the space itself changes through the addition of new genes and new characters.

The first steps toward ameliorating the lack of a theory of evolutionary novelty came from work on gene duplication, which looked at the origin of new genes rather than allelic variation at existing loci. The mathematical structure of gene duplication models and general representations of novel characters is quite different from the representations used in classical population and quantitative genetics, and recent progress has been made in defining the properties of 'evolutionary space' where the number of dimensions (characters, as opposed to states of a fixed number of characters) is itself fluid.

However, because the mathematical language of Neo-Darwinism was incomplete from the standpoint of describing evolutionary novelty, this does not imply that the biological mechanisms involved in morphological and genetic innovations are unknown and outside the scope of genetics. In a sense, the problem is analogous to the state of speciation theory in the first half of the twentieth century - while speciation (and evolutionary novelty) may not required any novel genetic or evolutionary mechanisms as explainations, the existing paradigm failed to incorporate these phenomena, because in the first case classical population genetics did not ask questions about the origin of isolating mechanisms, and in the second case it did not ask questions about how to represent the loss or gain of traits in the traditional framework.

As to the underlying mechanisms involved in the origin of evolutionary novelty, most of the current explanations focus on two classes of genetic phenomena: gene duplication and developmental regulatory genes. In the former case, the duplication of a gene through various means (such as unequal crossover or gene conversion) creates genetic redundancy that at least in principle permits one copy to take on novel functions while the duplicate maintains its original function. This allows for the origin of novelty without counteradaptive macro-mutational changes. A noteworthy and familiar example is the globin gene family in vertebrates, where gene duplication has allowed these oxygen-carrying molecules to evolve specialized functions such as fetal hemoglobin in mammals.

The other main empirical contribution to the understanding of evolutionary novelty is the discovery of regulatory genes (such as Hox genes in animals) that control the activation and timing of downstream regulatory cascades. Such genes have the property that a single locus mutation can have drastic phenotypic consequences. The evolution of Hox and other regulatory genes is also full of examples where one regulatory gene co-opts the function of others or is recruited in an entirely new function.

While many mutations in such regulatory genes are deleterious if not outright lethal, a number of experimentally induced Hox mutations in Drosophila and other laboratory animals have produced morphological variants (such as additional pairs of wings in normally two-winged flies, or limbs in place of antennae) that resemble the morphologies of distantly related taxa. For example, it is likely that the small amount of overall genetic difference between humans and great apes, which is observed in spite of the great morphological and behavioral differences, is quite typical of macroevolutionary changes in morphology. Specifically, mutations in a small number of regulatory genes lead to significant phenotypic divergence, including the losses of key traits such as appendages, change in their position, and sometimes even the seemingly de novo acquisition of traits.

Consequently, just as adaptive radiations can be seen as a special case of speciation and adaptive evolution under certain fitness landscapes, so large-scale changes in phenotype can be seen as special case of mutation and selection in regulatory genes.

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