Historical Constraints and the Evolution of Development 1099
Myriapoda and, for that matter, in the equally homonomous sister phylum of
onychophorans (Grenier et al., 1997). De Rosa et al. (1999) conclude that the full
complement must be even more ancient, as phyletic analysis indicates a minimum of
7 Hox genes for the bilaterian ancestor, and at least 8 for the common ancestor of
protostome phyla.
Thus, the differentiation of distinctive bilaterian body plans has occurred not by
the duplication or recruitment of additional Hox genes, but by changes in their
regulation and their downstream targets. Presumably, Hox genes "read" positional
information to set the location of differentiating structures, thereby triggering the
cascade of downsteam architects, but not building the varied structures themselves.
As Warren et al. (1994, p. 461) write: Hox genes "provided a pre-existing groundplan
upon which insect segmental diversity evolved." Carroll (1995, p. 483) therefore
restated the Lewis hypothesis as follows: "What has evolved in the course of insect
and fly evolution are not new genes but new regulatory interactions between BX-C
proteins and genes involved in limb formation and wing morphogenesis."
The discovery of the homeobox—a 180 base pair unit coding for a 60 amino
acid homeodomain with important regulatory action as a DNA binding protein—as a
common constituent of Hox genes (and others as well) opened the floodgates of this
amazingly fruitful research in the early 1980's. By probing for homeoboxes, Hox
genes could quickly be located and characterized, and (even more crucially for
evolutionary analysis) their homology to genes of other organisms (even in other
phyla) established. The two homeotic complexes of Drosophila—Antennapedia
(ANT-C) and Bithorax (BX-C)— were quickly revealed as separated subunits,
controlling the positioning of anterior and posterior structures along the A-P axis
respectively, of a single Hox cluster that maintains its integrity in the beetle
Tribolium, and in other nondipteran insects. Powers et al. (2000) show that the
mosquito Anopheles gambiae also retains a single and undivided Hox cluster, so the
Drosophila subdivision does not characterize Diptera in general.
The established rules of "hoxology"* vindicated the central principles of
morphogenesis in Lewis's model, though under an interestingly different genetic
regime. (The BX-C component of the Drosophila Hox sequence contains only three
genes, and if they arose, one from the other, by tandem duplication, these events
probably preceded the separation of protostome and deuterostome phyla.) But Lewis
could not have been more prescient in recognizing the essential sequence and form of
Hox action, and in specifying the implied consequences and tests. Lewis's principle
established the basis for discovering homologous genes (and homologous actions) in
distant groups, thus potentiating evo-devo's greatest and most surprising discovery of
"deep homology" among animal phyla—the key to the reevaluation of
- The verbal pun upon "doxology"—the short, formulaic, and unvarying, prayers of
Christian liturgy—inevitably comes to mind, although we trust that the norms of science
will prevail to impose substantial and interesting improvements upon the current hoxology.