Historical Constraints and the Evolution of Development 1113
As for limbs, I will argue in the next section (pp. 1134-1142) that the putative
homology of some genetic pathways resides in such generalized rules of
morphological organization (for the initiation of any "outpouching" orthogonal to a
major axis, for example) that little support for particular historical constraints can be
drawn from the claim for genetic retention. (After all, properties so pervasive and
general as the structure of DNA, or so broad as the necessary physical geometry of
elongation and outpouching, do not manifest the specificity required to identify
limitations or channels arising from definite historical positions on life's phyletic
tree.)
As for the vertebrate head, current knowledge favors a status even less congenial
to claims for homology across phyla, and to strong historical constraint: interpretation
of this definitive vertebrate structure as a true novelty and neomorph, and not as a
highly modified organ constructed from parts homologous to units of the arthropod
Bauplan. The foundation of this argument rests upon distinctive features of the
vertebrate neural crest and its astonishing range of developmental derivatives and
influences (Gans and Northcutt, 1983). Thus, despite important homologies in
products of the developing hindbrain and its rhombomeres, the vertebrate mid and
forebrain seems to represent a largely "suradded" structure, unique to the vertebrate
(or at least to the chordate) lineage.
I do not challenge this general argument, but some aspects of the vertebrate fore
and midbrain may exhibit developmental homology with anterior segmentation in
protostome phyla. In particular (see Simeone et al., 1992; Holland et al., 1992; and
Raff, 1996, pp. 199-200), the Drosophila gap genes orthodenticle (otd) and empty
spiracles (ems) operate in the establishment of head segmentation at the fly's front
end, anterior to the domain of expression for Hox genes. Two homologs of each of
these homeobox genes (Otx1 and 2, and Emx1 and 2) have now been identified in
mice, and their domain of action also maps to the forebrain and midbrain, anterior to
the expression of Hox genes in the rhombomeres of the hindbrain (see Fig. 10-17,
taken from Holland et al., 1992, p. 627). But we do not yet know if these genes
encode common modes of action (in addition to their similarity in genetic structure
and locus of operation).
On this chapter's central subject of degrees of constraint, Holland et al. (1992)
offer the interesting suggestion that these gap gene homologies might enforce less
channeling upon patterns of development than the Hox genes impose, and that the
greater independence, flexibility and subsequent novelty and variety of the vertebrate
head might flow, in part, from the absence of more constraining Hox action in the
mid and forebrain regions. (In particular, as Figure 10-17 illustrates, "the four Otx
and Emx genes show a nested series of posterior expression boundaries, in contrast to
clearly nested anterior expression boundaries in the Hox genes" (Holland et al., 1992,
p. 627.) Moreover, whereas the anatomical expression of Hox genes strictly parallels
their spatial order on the chromosome, Otx and Emx show no evidence for similar
clustering in the genome). Holland et al. (1992, p. 628) therefore hypothesize: