Historical Constraints and the Evolution of Development 1167
But this reasonable conjecture was then falsified because, just as in dipterans,
Ubx does not turn on in the lepidopteran forewing imaginal disc, but achieves high
levels of expression in the hindwing disc. Therefore, the growth of lepidopteran
hindwings in the presence of Ubx must depend upon differences in the downstream
T3 cascade of flies vs. butterflies. Warren et al. (1994, p. 461) conclude: "The most
logical explanation is that the sets of downstream wing-patterning genes regulated by
Ubx in these orders have diverged. In this view, Ubx operates in butterflies upon
pattern regulating genes to differentiate hindwings from forewings, and in flies upon
a different set of genes to distinguish halteres from wings."
In further confirmation from detailed patterns at lower taxonomic levels,
Weatherbee et al. (1999) then studied Hindsight, a homeotic mutation in butterflies
that transforms parts of the hindwing into forewing identity. They found that these
hindwing transformations in color and scale morphology occur in regions of the
forewing where Ubx expression has been lost, thus sensibly explaining, under the
general rule for Hox expression in butterfly wings, the apparent forewing identities of
these altered regions. Reemphasizing the important principle previously illustrated
for echinoderms vs. other triploblast phyla, but at this lower taxonomic level—that
channels of internal homology also promote flexibility, not just limitation, through
such mechanisms as cooptation and diversification of downstream cascades—
Weather-bee et al. (1999, p. 113) write: "The diversity of insect hindwing patterns
illustrates the broad range of possible morphologies that can evolve in homologous
structures that are regulated by the same Hox gene."
I turn, finally, to the two canonical and most anatomically extensive examples of
evolution from homonomy to regional specialization and complexity in the evolution
of insects and other arthropods—evolution from the plesiomorphic state of walking
legs on all post-oral segments and, for pterygotes, from the ancestral condition (as
revealed in the fossil record and preserved in modern mayfly larvae) of wings on all
thoracic and abdominal segments. Data from evo-devo have effectively resolved the
old debate about whether insect wings evolved as novel structures from hypothesized
rigid extensions of the body wall in terrestrial forebears (the paranotal theory), or
from dorsal branches of polyramous appendages of ancestral forms (the limb-exite
theory).
Genetic data support the exite theory and provide a fascinating example of
cooptation in evolution (the general subject of the subsequent Chapter 11). In the
exite theory, insect wings and legs are, in some sense, serially homologous as
specializations of different parts of an ancestral polyramous appendage— the wings
from the dorsalmost branch (the exite) and the leg from the ventralmost-walking
branch. In their major topological difference, wings develop as sheets, and legs as
tubes. In Drosophila, the wing grows under the crucial influence of apterous, which
is expressed only in dorsal cells and therefore maintains clear distinction between
dorsal and ventral surfaces, thus abetting the growth of a sheet-like structure (Shubin
et al., 1997). But the apterous gene does not function in the growth of tubular legs in
Drosophila. However,