Independent genetic representation of functionally distinct character complexes can be described as modularity of the genotype-phenotype mapping functions. A modular representation of two character complexes C1 and C2 is given if pleiotropic effects of the genes fall mainly among members of the same character complex, and are less frequent between members of different complexes (see Fig. 1). This depiction should be understood as mainly illustrative, because a full and quantitative characterization of modularity would have to allow for hierarchies, gradations, and overlapping of modules. The development of a quantitative characterization of modularity is a part of the research program advocated here.
Some adaptations may intrinsically have a modular genetic representation because they are simple, and involve direct gene action. Examples include immunoglobulin antigen binding, hair color, enzyme activity, etc.. These are functions with low polygeny and low pleiotropy. Morphogenesis presents the greatest challenge in producing a modular representation because it is a dynamical system emerging from the complex interactions of many genes and structures. Modularity in morphogenesis is facilitated by at least one intrinsic property, the branching structure of clonal lineages and spatial proximity initially shared by a clone of differentiating cells. But the ontogeny of many functional complexes involves interactions between distantly diverged clones, and again modularity becomes a property to be explained rather than a given. The challenge that morphogensis presents in achieving a modular genotype-phenotype map perhaps explains why most of the study of the genotype-phenotype map has been undertaken by evolutionary morphologists.
The concept of modularity was clearly expressed by John Bonner in his concept of gene nets (Bonner, 1988):
The idea that development is organized into semi-autonomous processes is actually much older, dating back to the beginnings of developmental biology and was summarized under the term "dissociability" by Needham (1933). Needham pointed out that even if development is a perfectly integrated process its component parts can be disentangled experimentally: growth can occur without differentiation and nuclear division without cell division and so on. The evolutionary importance of this fact was emphasized by Gould (1977, p 234) who suggested that dissociability is the developmental prerequisite for heterochronic change (see also Raff and Kaufman, 1983, p 150, Raff, in press).
Evolution of complex adaptations requires a match between the functional relationships of the phenotypic characters and their genetic representation. This was clearly expressed by Rupert Riedl (1975) in his thesis of the "imitatory epigenotype." If the epigenetic regulation of gene expression "imitates" the functional organization of the traits then the improvement by mutation and selection is facilitated. Riedl predicts that selection tends to favor those genotype-phenotype maps which imitate the functional organization of the characters. Imitation means that complexes of functionally related characters shall be "coded" as developmentally integrated characters but coded independently of functionally distinct character complexes (see also Frazzetta, 1975).
The existence of semi-autonomous units of the phenotype might be particularly important in connection with sexual reproduction (Stearns, 1993). Sexual reproduction rearranges genetic variation in every generation which creates the problem of maintaining functional phenotypic units intact. Stabilizing the development of functionally related character complexes allows the recombination of integrated traits rather than true "random" variation.
The fact that the morphological phenotype can to a great extend be decomposed into basic organizational units, the homologues of comparative anatomy, has also been explained in terms of modularity. It has been suggested that properly identified homologues are developmentally and genetically individualized parts of the organisms (Wagner, 1989b,c). The biological significance of these semi-autonomous units is their possible role as "building blocks" of phenotypic adaptation (Wagner, 1995a).
Figure:
Example of a modular representation of the character complexes C1={A, B, C, D}
and C2={E, F, G} which serve to functions F1 and F2.
Each character complex has a primary function, F1 for C1 and F2 for C2.
Only weak influences exist of C1 on F2 and vice versa. The genetic
representation is modular because the pleiotropic effects of the
genes M1={G1, G2, G3} have primarily pleiotropic effects on the
characters in C1 and M2={G4, G5, G6} on the characters in complex C2.
There are more pleiotropic effects on the characters within each complex
than between them.