Historical Constraints and the Evolution of Development 1165
ancient form suggests that regional repression of Hox gene expression could
have played a role in the evolution of the vertebral column... We propose
that, in antecedent vertebrates, Hox genes involved in patterning the axial
skeleton were expressed in relatively broad regions of paraxial mesoderm.
The resulting less complex Hox code would have established the similar
vertebral identities observed in broad regions of early vertebrate skeletons.
Regionalization of the vertebral column subsequently evolved in concert with
the evolution of restricted patterns of Hox gene expression in paraxial
mesoderm.When we turn to specific examples in the evolution of differentiated and
complexified axial structures in arthropods and vertebrates, we commonly find
correlations between morphological inventions and the restriction and regionalization
of Hox gene expression. I have already discussed several cases in previous sections of
this chapter—particularly the complex and elegantly documented story of multiple
parallel evolution of crustacean maxillipeds from ancestral limbs that were more
homonomous with the rest of the posterior thoracic series. This complexification
originates by suppression of Ubx and abdA in just those anterior thoracic segments
that develop maxillipeds in each case.
Enlarging upon this example, Averof and Akam (1995) found that three middle
Hox genes—Antp, Ubx and abdA—"are expressed in largely overlapping domains in
the uniform thoracic region" of branchiopod crustaceans (1995, p. 420, and see Fig.
10 - 27). In the more highly differentiated insects, on the other hand, the same three
genes show more restricted expression in discrete domains, where "they specify
distinct segment types within the thorax and abdomen" (p. 420). In particular, Antp
turns on in thoracic segments (that develop legs and wings) but not in abdominal
segments. Similarly, both Vbx and abdA are expressed in all abdominal segments,
where they repress distal-less and therefore presumably regulate the repression of
legs on all abdominal segments.
In an elegant affirmation that has already become a classic of the evo-devo
literature, Warren et al. (1994) demonstrated that lepidopteran larvae develop prolegs
on their abdominal segments by localized deletion of Ubx and abdA expression,
followed by subsequent derepression of distal-less in the small bilateral patches on
each abdominal segment, from which the prolegs then grow. They conclude (1994, p.
458) that "abdominal limb formation in butterflies has been made possible by the
evolution of a regulatory mechanism for shutting off these two BX-C [Hox in modern
terminology] genes in selected cell populations, which then permits Dll and Antp to
be expressed."
Warren et al. then raise an obvious question that exemplifies a related principle
in the evolution of differentiated complexity from homonomous ancestry: Why didn't
butterflies evolve their abdominal prolegs by the "easier" route of fixing a Dll
mutation to release repression by Ubx and abdA? Why follow the more complex
scenario of first repressing the two Hox genes in local patches, and then permitting
the ordinary action of Dll? Warren et al. offer