Even if the fact and importance of modularity has a long historical tradition, there is little understanding of how modularity has originated. Is it an inherent property of organisms and thus not the result of evolution in the Darwinian sense or is it the result of selection shaping the genotype-phenotype mapping function? Is modularity the result of integrating disconnected parts or, on the contrary, the result of parcellation of primarily integrated parts. Parcellation, a process which produces modularity from an integrated whole, consists in the differential suppression of pleiotropic effects among characters belonging to different complexes and the selective maintenance and augmentation of pleiotropic effects among the members of the same complex (Fig 2).
The first possibility, that modularity is a primitive property of all living beings, is unlikely. As much as the evolution of higher organisms consists in the acquisition of modular parts, like specialized organs the origin of modularity is most likely the result of evolutionary modification.
Figure 2:
Two ways of obtaining modularity. Parcellation consists of a differential suppression of pleiotropic effects between groups of characters and the maintenance and/or augmentation of pleiotropic effects among characters from the same group. Modularity through integration consists in the selective acquisition of pleiotropy among characters from the same group.
As to the 'direction' of evolution, integration or parcellation of modules (Fig. 2), the most prevalent direction seems to be parcellation, at least among metazoan animals. The origin of metazoans is the integration of conspecific unicellular individuals into a higher level unit (see Buss, 1987). Each of these units consists of cells which have the same genotype and only secondarily organize in specialized cell populations and anatomically separated organs. A very frequent mode of morphological innovation is the differentiation of repeated elements (Müller and Wagner, 1991; Weiss, 1990), for instance the differentiation of metameric segments at the origin of insects (see for instance Akam, 1989). The specialized organs acquire developmental autonomy in the course of phylogeny (Bonner, 1988). Hence, the origin of differentiated, complex animals appears to be dominated by the process of parcellation rather than secondary integration, even if integration certainly occurs, for instance in symbiotic integration of cells of different origin (mitochondria and plastids for instance).
Provided that modularity is most likely the derived state in the phylogeny of animals and is perhaps the result of parcellation rather than integration, the question arises of how parcellation has been caused by natural selection. Perhaps the most common and long lasting form of selection experienced by any species is stabilizing selection (Endler, 1986). However, stabilizing selection alone is the least likely candidate for causing parcellation. Stabilizing selection on all characters simultaneously favors suppression of all mutational effects (Wagner, submitted). It is thus unlikely to lead to modularity.
Two other mechanisms have been proposed: selection for adaptation rate (Rechenberg, 1973; Riedl, 1975) and "constructional" selection (Altenberg, 1994). Selection for adaptation rate assumes that modular or otherwise favorable representations of the phenotype will get selected because they are able to respond more quickly to directional selection. This is indeed the case and can happen without group selection (Wagner, 1981). However, the problem is that selection for adaptation rate requires high degrees of linkage disequilibrium (Wagner and Bürger, 1985) and is only effective in the absence of recombination. The reason is that recombination during sexual reproduction leads to a mixing of genotypes and thereby eradicates the adaptive advantages achieved by genotypes with a better genetic representation (Wagner, unpublished).
The second proposal suggests that modularity evolves during genome growth by gene duplication (Altenberg, 1994). This highly original proposal suggests that duplications of genes with fewer pleiotropic effects are more likely to be viable than duplications of genes with many pleiotropic effects. Indeed simulations have shown that such a process would lead to modular organizations, provided that gene duplications are associated with direct effects on fitness (Altenberg, 1994).
Another possibility of sufficient generality is that the combination of directional and stabilizing selection leads to the differential suppression of pleiotropic effects (Wagner, in preparation). This proposal assumes that adaptation to environmental perturbations includes directional selection on one or a few functions or character complexes (mosaic evolution). It implies that directional selection on adaptively challenged character complexes occurs simultaneously with stabilizing selection on all the other characters. This combination of selection forces creates strong selection for suppressing exactly those pleiotropic effects which connect the characters under different selection regimes (directional and stabilizing). Simulation studies show that the selection coefficient of a gene suppressing pleiotropy among adapting (= under directional selection) and non-adapting characters (= under stabilizing selection) can be up to 0.3 depending on the intensity of directional selection and the strength of stabilizing selection (Wagner, in preparation). However, it is not yet clear what the necessary conditions are under which this process is a likely explanation of modularity, and whether these conditions are realized in nature. More research into the population genetic theory of genotype-phenotype mapping functions is necessary to assess the plausibility of this and the other scenarios to explain the evolution of modularity. More knowledge of the developmental and evolutionary processes underlying the origin of modular parts of organisms is required to understand the significance of modularity.