The Questions of Developmental Biology

Modularity: The Prerequisite for Evolution through Development
How can the development of an embryo change when development is so finely tuned and
complex? How can such change occur without destroying the entire organism? It was once
thought that the only way to promote evolution was to add a step to the end of embryonic
development, but we now know that even early stages can be altered to produce evolutionary
novelties. The reason why changes in development can occur is that the embryo, like the adult
organism, is composed of modules (Riedl 1978; Bonner 1988).
Development occurs through a series of discrete and interacting modules (Riedl 1978;
Gilbert et al. 1996; Raff 1996; Wagner 1996). Organisms are constructed of units that are
coherent within themselves and yet part of a larger unit. Thus, cells are parts of tissues, which are
parts of organs, which are parts of systems, and so on. Such a hierarchically nested system has
been called a level-interactive modular array (Dyke 1988). In development, such modules include
morphogenetic fields (for example, those described for the limb or eye), pathways (such as those
mentioned above), imaginal discs, cell lineages (such as the inner cell mass or trophoblast), insect
parasegments, and vertebrate organ rudiments. Modular units allow certain parts of the body to
change without interfering with the functions of other parts.
The fundamental principle of modularity allows three processes to alter development:
dissociation, duplication and divergence, and co-option (Raff 1996). Since modules are found on
all levels, from molecular to organismal, it is not surprising that one sees these principles
operating at all levels of development.
Dissociation: Heterochrony and allometry
Not all parts of the embryo are connected to one another. One can dissect out the limb
field of a salamander neurula, for example, and the eyes are not affected. By means of mutation
or environmental perturbation, one part of the embryo can change without the other parts
changing. This modularity of development can allow changes that are either spatial or temporal.
Heterochrony is a shift in the relative timing of two
developmental processes from one generation to the next. In other
words, one module can change its time of expression relative to the
other modules of the embryo. We have come across this concept in
our discussion of neoteny and progenesis in salamanders (see
Chapter 18). Heterochrony can be caused in different ways.
In salamander heterochronies in which the larval stage is retained,
heterochrony is caused by gene mutations in the ability to induce or
respond to the hormones initiating metamorphosis. Other heterochronic phenotypes, however, are
caused by the heterochronic expression of certain genes. The direct development of some sea
urchins involves the early activation of adult genes and the suppression of larval gene expression
(Raff and Wray 1989). Thus, heterochrony can "return" an organism to a larval state, free from
the specialized adaptations of the adult. Heterochrony can also give larval characteristics to an
adult organism, as in the small size and webbed feet of arboreal salamanders (Figure 22.17) or the
fetal growth rate of human newborn brain tissue (see Chapter 12).
Another consequence of modularity is allometry. Allometry occurs when different parts
of an organism grow at different rates (see Chapter 1). Allometry can be very important in
forming variant body plans within a phylum. Such differential growth changes can involve