1148 THE STRUCTURE OF EVOLUTIONARY THEORY
at first—if only because most of us can only imagine so much novelty at once. As
discussed before in different contexts, when Ed Lewis (1978) recognized the Hox
genes as linearly ordered in both space and time, and inferred their origin by tandem
duplication from a precursor, he interpreted the evolutionary significance of these
amplifications in an "obvious" and conventional manner (the proper "first pass"
procedure in science, and therefore recalled here without critical intent, while noting
that our later explanatory reversal only underscores the importance of Lewis's
discovery). Lewis proposed that the addition of duplicated Hox genes could be
directly and causally correlated with the specialization and differentiation of
appendages along the arthropod AP axis, as an originally homonomous ancestor
evolved into the diverse Bauplan of major arthropod taxa. In particular, Lewis argued
that an addition of Hox genes allowed evolving members of the insect line to
suppress the growth of legs on the abdominal segments, and (in Diptera) to convert
the wings of the second thoracic segment to halteres. Lewis's original scenario
matches our conventional view of evolution, and of complex systems in general—
particularly in the assumption that a history of increasing elaboration in overt
products (the phenotypes of complex bilaterian phyla) should be underlain by a
growth in the number and intricacy of generating factors (genes regulating
developmental outcomes).
In one of the most important early discoveries of evo-devo, this entirely
reasonable scenario has been overturned and, in large measure, reversed. Two strong
sources of evidence now indicate that a full complement of Hox genes had already
evolved in the presumably homonomous common ancestor, not only of the
protostome phyla, but of the entire bilaterian line (thus further exemplifying the
homologies of arthropods and vertebrates). The multiple and independent evolution
from homonomy towards complexly specialized and differentiated Bauplan in several
phyla did not entail any increase in the number of Hox genes, but rather a
regionalization and decrease in the range of action of individual genes and,
especially, changes in both the regulation and content of the downstream cascades
differently engaged by the various Hox genes.
- Modern homonomous organisms share the full complement of Hox genes
with closest relatives among classically differentiated invertebrates. The genome of
myriapods, the homonomous sister group of insects for example, includes a full set of
insect Hox homologs (Raff, 1996). At the higher level of a sister group to the entire
arthropod phylum, the undoubted "standard" for highly differentiated body plans
along the AP axis, the genome of the homonomous Onychophora also includes all
insect Hox genes, as well as an ortholog of the pair-rule gene fushi tarazu (Grenier et
al., 1997). (Modern onychophores include only a few Gondwana species, restricted to
moist terrestrial habitats. The generic name of the most famous modern form,
Peripatus, honors the homonomy of the numerous lobopods, the pair of leglike
structures on each segment. But the Onychophora included a prominent and diverse
group of marine representatives in the earliest faunas of the Cambrian period.)
Grenier et al. (1997, p. 549) conclude that "the segmental