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ABSTRACT
Five nominal elements comprise the circumorbital series of bones in
gekkotans: prefrontal, postfrontal, postorbital, jugal, and lacrimal. Determination of the homology of two of these, the postfrontal and postorbital,
has been particularly problematic. Two conicting hypothesis exist relating
to these: either the postorbital is lost and the postfrontal remains or they
fuse during development to form a combined element, the postorbitofrontal. Such a combined element apparently occurs in at least some members
of all lizard clades. There is, however, no direct developmental evidence
that supports either theory. To overcome that, we investigate the sequence
and pattern of ossication in the circumorbital region in a developmental
series of the Leopard gecko. We posit that both the postfrontal and postorbital appear during development. Contrary to previous predictions they
neither fuses to each other, nor do either degenerate. Instead, the postfrontal shifts anteriorly and fuses with the frontal to become indistinguishable
from it by the time of hatching, and the postorbital persists as a robust independent element bounding the frontoparietal suture. These observations
accord, in part, with both hypotheses of homology of these elements and
result in the recognition of a new pattern, placing in doubt the existence of
the composite postorbitofrontal. The phylogenetic implications of these
ndings may prove to be far reaching if similar and conserved patterns of
development are encountered in other clades. Anat Rec, 293:20012006,
C 2010 Wiley-Liss, Inc.
2010. V
2002
EUBLEPHARIS
2003
CIRCUMORBITAL BONES
Fig. 2. The right postorbital of Eublepharis macularius in dorsolateral view, from the initiation of ossication in Stage 35 (A), through Stages 36 (B), 37 (C), 38 (DF), 39 (G), 40 (H), and 42 (I) (staging according
to Wise et al., 2009). Abbreviations: ap, anterior process; fprs, frontoparietal suture; lp, lateral process;
par, parietal; po, postorbital; pp, posterior process. Scale bar in each panel is 1 mm.
RESULTS
An ossication center occupying the classical position
of a postfrontal (Fig. 1A) (Conrad, 2008; Daza and
Bauer, 2010) rst appears as a small triangular center
in late Stage 35 (Fig. 2A). The base of this triangle is
oriented medially and straddles the future suture
between the frontal and parietal. It continues to enlarge
throughout Stages 35 and 36 (Fig. 2A,B). By Stage 37
(Fig. 2C) an anterior process that ultimately becomes
the part of the element that borders the frontal is evident. Both the triangle and anterior process continue to
grow throughout Stage 38 (Fig. 2DF), and by mid-Stage
38 (Fig. 2E), its lateral and caudal processes begin to
extend. By late Stage 38, its anterior process is complete
in terms of its adult proportional length, and ossication
of its lateral process has extended, producing a spike
(Fig. 2F), yielding a triradiate element. Stages 39 and 40
witness an increase in size without any concomitant
change in form (Fig. 2G,H). In Stage 41 (not illustrated),
the posterior process has widened to achieve its denitive
shape. By late Stage 42 (Fig. 2I), the anterior process of
the postorbital is still pointed and spike-like and has not
yet gained the wide, blunt form of mature specimens.
Lying slightly anterior to the aforementioned element,
but still separating its rostral portion from contact with
the frontal, another ossication center that occupies a
position anterior to the triangular element lying
2004
DISCUSSION
Our observations accord in part with the predictions
derived from the hypotheses of both Evans (2008) and
Daza and Bauer (2010). The former predicts that the
postfrontal should appear as a single center and remain
as a single center throughout development, and that the
postorbital will either not appear or will appear and
then lose its individual identity (but will not fuse to the
postfrontal). This is partly borne out. The element
regarded as the postfrontal by Evans (2008) appears and
develops as a single center, but actually has all of the
morphological characteristics of the primitive gekkotan
postorbital (Conrad and Norell, 2006) (Fig. 2) but lying
in a more dorsomedial position, bounding the frontoparietal suture. An additional element, however, lying anterior to this appears, but quickly fuses to the lateral edge
of the frontal in the dorsal rim of the orbit (Fig. 3). This
element lies more anterior than the location of the primitive gekkotan position for the postfrontal (see illustrations in Conrad and Norell, 2006), and lacks the lateral
process of that element, but still separates the rostral
portion of the postorbital from contact with the frontal.
We advocate that it is more parsimonious to propose an
anterior shift of an existing element than the appearance of a de novo structure and the loss of another.
Here, the postfrontal and the postorbital maintain a
close position relative to one another, but with the loss
of the postorbital bar and upper temporal arch, characteristic of more derived gekkotans, there is a dorsomedial and rostral shift with respect to their relationship
to the less labile elements comprising the skull roong
bones, namely the frontal and the parietal.
Predictions resulting from Daza and Bauers (2010)
hypothesis indicate that ossication centers for the postfrontal and postorbital should both appear and then
Fig. 3. The postfrontal of E. macularius from (A) initiation of ossication in late Stage 36 to complete fusion with the frontal (E) in Stage
40 (staging according to Wise et al., 2009). Panels AC are in dorsolateral view; D and E are dorsal views, and rostral is to the right in all
views. AC and E depict elements of the right side; D depicts elements from the left. Anterior is to the right. A, later Stage 36; B and C,
Stage 38; D, Stage 39; E, Stage 40. The white arrow in AD demar-
cates the rostral end of the postfrontal and the white arrowhead the
caudal end. The white and black arrowheads demarcate the point of
fusion between the caudal end of the postfrontal and the barb of
the frontal. The black arrow in panel D demarcates the overlap of the
prefrontal and postfrontal. Abbreviations: fps, frontoparietal suture;
par, parietal; pfr, postfrontal; po, postorbital; pref, prefrontal. Scale bar
represents 1 mm.
2006
also be interpreted as the retention of the primitive location of the postfrontal and an anterior shift of the postorbitalthe blue and yellow color coding on Fig. 1D
would be switched to depict this). The second interpretation outlined above requires the additional developmental events of a de novo ossication (the splint-like
element) and the loss of an element (the postorbital).
The third alternative would require the same de novo
addition and the fusion of two elements for which there
is no developmental evidence.
The ve developmental stages (range, 3640) over
which the initiation of ossication of the postfrontal (our
preferred interpretationsee above) and its subsequent
fusion to the frontal occur cover a time span that can
vary from 8 to 14 days (Wise et al., 2009). Dense sampling of embryos over these developmental stages permitted the observation of critical but transient events.
The phylogenetic implications of these data may be
more far reaching within the Squamata, because
detailed information about potentially transient events
in skull development are scarce. The widespread recognition of a postorbitofrontal in most squamate lineages
may hinge upon assumptions about fusion of elements
(Bellairs and Kamal, 1981) for which there is little evidence. This sporadic occurrence of putative fusion of the
postorbital and postfrontal is homoplasious, and thus
convergent. If the pattern observed in Eublepharis is
more widespread in its distribution, then alternate
explanations would pertain (although these may not
reduce the incidence of homoplasy).
We echo the recommendations of Daza and Bauer
(2010) that particular attention should be given to patterns of ossication in this cranial region across the
Squamata. Questions of homology can only be resolved
through the acquisition of details of embryonic development gained from densely sampled appropriate periods
of prehatching development.
LITERATURE CITED
Bellairs AdA, Kamal M. 1981. The chondrocranium and the development of the skull in recent reptiles. In: Gans C, Parsons TS,
editors. Biology of the Reptilia, Vol. 11. Morphology F. London:
Academic Press. p 1263.