The Questions of Developmental Biology

Assessing Homologies through Regulatory Gene Expression Patterns
What constitutes a spider's head?
Once a typical pattern of expression has been determined for genes such as those of the
Hox complex, one can attempt to derive the evolution of anomalous structures by looking at their
patterns of gene expression. For instance, chelicerates (spiders and mites) are very derived
arthropods. They do not have a distinct head, but rather a cephalothorax, and it is difficult to see
the segmentation in their brains. While their heads and brains may look very different from those
of insects, the expression pattern of Hox genes in the anterior of the spider embryo is very similar
to that in the head of an insect embryo. This pattern demonstrates that spiders have the same head
segments as insects and therefore supports the view that all arthropods (of which chelicerates and
insects are members) have a common origin (Damen et al. 1998; Telford and Thomas 1998).
How does a new cell type form?
As mentioned earlier in the chapter, the neural crest cells were important in the origin of
chordates. While we do not know how neural crest cells arose, Holland and colleagues (1996)
have provided a fascinating speculation that involves the duplication and divergence of new
genes. It also involves the vertebrate homologues of the Drosophila gene Distal-less. Distal-less is
found throughout the animal kingdom, and it is expressed in those tissues that stick out from the
body axis, notably limbs and antennae (Panganiban et al. 1997). But in vertebrates, Distal-less has
acquired new functions. Amphioxus is an invertebrate chordate that has a notochord, somites, and
a hollow neural tube. It lacks a brain and facial structures, and most importantly, it lacks neural
crest cells. Like Drosophila, amphioxus has but one copy of the Distal-less gene per haploid
genome, and as in Drosophila, this gene is expressed in the epidermis and central nervous system.
However, whereas amphioxus has only one copy of this gene, vertebrates have five or six closely
related copies of Distal-less, all of which probably originated from a single ancestral gene that
resembles the one in amphioxus (Price 1993; Boncinelli 1994). These Distal-less homologues
have found new functions. Some are expressed in the mesoderm, a place where Distal-less is not
expressed in amphioxus. Other vertebrate Distal-less homologues are expressed in the forebrain,
mimicking an expression pattern seen in the anterior of the amphioxus neural tube.
These findings suggest that the vertebrate forebrain is homologous to the anterior neural tube of
amphioxus. At least three of these vertebrate Distal-less genes function in the patterning of the
neural crest cells, and deletions of these genes cause the absence or malformation of the branchial
arches, face, jaws, teeth, and vestibular apparatus (Qiu et al. 1997; DePew et al. 1999).
Although it remains unproved, it is possible that the new type of Distal-less gene could have
caused the migratory ectodermal cells of amphioxus to evolve into neural crest cells.
Is the endostyle the precursor of the thyroid gland?
Similarly, there has been disagreement as to whether the endostyle of amphioxus is
homologous to the thyroid gland of vertebrates. Both organs accumulate iodine, although the
endocrine function of the endostyle has not been demonstrated. Recent studies (Holland and
Holland 1999) have shown that in addition to its structural and functional similarities to the
vertebrate thyroid, the endostyle also expresses two transcription factors that are used to specify
the vertebrate thyroid. Therefore, the case for homology between these two organs is
strengthened.