Historical Constraints and the Evolution of Development 1141
1997, p. 645). The vertebrate limb develops in a similar way under homologous
influences. Sonic Hedgehog (Shh), a homolog of Drosophila hedgehog, is also
located in the posterior part of the limb bud, and also induces a homolog of dpp,
called Bmp- 2 in its vertebrate version, which then acts in differentiating the AP axis.
Interestingly, and in a striking confirmation of important homology in function as
well as structure, misexpression of either Shh or hedgehog on the anterior rather than
the posterior edge of the developing appendage causes the same striking
malformation: mirror image duplications at the anterior border.
In organizing the proximodistal structure of the Drosophila wing, a specialized
set of cells, called the wing margin, runs along the DV border of the imaginal wing
disc. The fringe gene establishes the edge of the developing wing at the interface
between cells that do and do not express fringe. The vertebrate apical ectodermal
ridge (AER), like the Drosophila wing margin, also runs along the DV border of the
developing limb bud. Radical fringe, a vertebrate homolog of fringe, is also
expressed in the dorsal region limb ectoderm before the AER forms. Moreover, at the
border of cells that do and do not express radical fringe, Ser-2, a homologue of
Drosophila serrate (an important element in the downstream cascade regulated by
fringe) becomes expressed, and the AER then forms.
Data for the DV axis are less well developed, but "genes specifying DV polarity
in both groups have been identified" (Shubin et al., 1997, p. 646). For example, in
Drosophila, the expression of apterous helps to define the dorsal compartment of the
wing disc and also specifies dorsal cell fates. A related, but not clearly homologous
vertebrate gene, Lmx-1, defines a dorsal compartment of the vertebrate limb, and also
conveys dorsal cell fate.
Shubin et al. (1997, p. 646) summarize the evolutionary meaning of these
complex, column-like developmental constraints: "The simplest phylogenetic
implication to draw from these comparisons is that individual genes that are
expressed in the three orthogonal axes are more ancient than either insect or
vertebrate limbs ... either similar genetic circuits were convergently recruited to make
the limbs of different taxa or a set of these signaling and regulatory systems are
ancient and patterned a structure in the common ancestor of protostomes and
deuterostomes."
Their stated preference for the second alternative (Shubin et al., 1997, p. 647)
illustrates the intermediary character of this example, as recording too broad a
constraint to permit the identification of any particular vertebrate limb as "the same"
structure as any given arthropod appendage, but also as based upon a sufficiently
detailed and complex set of genetic homologies to set a common developmental
channel with more specificity than a Pharaonic brick, albeit not at the level of
constraint of a full Corinthian column: "This ancestral structure need not have been
homologous to arthropod or vertebrate limbs; the regulatory system could have
originally patterned any one of a number of outgrowths of the body wall in a
primitive bilaterian for example... The key step in animal limb evolution was the
establishment of an integrated genetic system to promote and pattern the development
of certain