1164 THE STRUCTURE OF EVOLUTIONARY THEORY
- Overexpression, in both position and amount, of vertebrate Hox genes has
generated atavisms in several experiments, thus suggesting that derived
specializations evolve by tighter regionalization and restriction of expression in
individual Hox genes. Pollock et al. (1995) studied the influence of over-expression
for Hoxb- 8 and Hoxc- 8 upon the skeletal development of mice, concluding that
"many of the morphological consequences of expanding the mesodermal domain and
magnitude of expression of either gene were atavistic" (p. 4492). For example, the
earliest Paleozoic vertebrates grew "free ribs" (independent from and articulating
with the vertebrae) along the entire body axis, from the base of the skull to the tail.
Many subsequent tetrapod lineages, particularly among mammals, reduced the
number of free ribs dramatically. But vestiges of the ancestral free ribs sometimes
remain as small units fused with the vertebrae. In particular, the lumbar
pleurapophyses of posterior mammalian vertebrae "most likely represent an ancestral
rib that has fused with the lateral portion of the vertebrae and now serves as a point of
attachment for muscle groups of the back" (p. 4495). Pollock et al. (1995)
documented "the reappearance of free ribs at the expense of lumbar pleurapophyses"
in Hoxb- 8 transgenic mice—"a clear example of atavism" (p. 4495). In another
experiment, mice developing with overexpression of both Hoxb- 8 and Hoxc- 8 grew
costal tubercles on their lower thoracic ribs. Costal tubercles represent a vestige of
the second head of the articulating boss in free ribs. Normal mice develop no costal
tubercles on these ribs at all.
In a similar experiment, Lufkin et al. (1992) ectopically expressed a Hoxd gene
"more rostrally than its normal mesoderm anterior boundary of expression" (p. 835)
at the level of the first cervical somites. This anomalous anterior expression generated
"a homeotic transformation of the occipital bones towards a more posterior phenotype
into structures that resemble cervical vertebrae" (p. 835). One should not read too
much evolutionary meaning into one experimental manipulation, but since the same
ectopic expression also induced other changes of a potentially atavistic nature
(particularly "the presence of clearly segmented neural arches arising from the most
anterior somites," p. 840), and since the vertebrate skull and forebrain probably arose
as novel features at the anterior end of a more homonomous ancestor, any
transformation of skull parts towards the phenotype of more homonomous posterior
vertebrae can hardly fail to elicit thoughts about the phylogeny of the vertebrate
skull—especially when these potential atavisms arise by reversing the presumed
phyletic restriction and posterior localization of Hox action. Lufkin et al. (1992), in
what I can only regard as an expression of chutzpah (but still worth pondering), even
ask: "Would ectopic expression of additional Hox genes be required to convert fully
the neurocranium into vertebrae?" (p. 840).
Pollock et al. (1995, pp. 4495-4496) also reach a bold conclusion that may go
too far, but that merits careful consideration:
The observation that expansion of the functional domain of a Hox gene can
result in the transformation of a modern costal structure to a more