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Development of the Dorsal Circumorbital Bones in the Leopard Gecko (Eublepharis macularius) and Its Bearing on the Homology of These Elements in the Gekkota.

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THE ANATOMICAL RECORD 293:2001–2006 (2010)
Development of the Dorsal
Circumorbital Bones in the Leopard
Gecko (Eublepharis macularius) and Its
Bearing on the Homology of These
Elements in the Gekkota
PATRICK ARTHUR DAVID WISE* AND ANTHONY PATRICK RUSSELL
Department of Biological Sciences, University of Calgary, Calgary, Alberta,
Canada T2N 1N4
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 conflicting 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 ossification 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
findings may prove to be far reaching if similar and conserved patterns of
development are encountered in other clades. Anat Rec, 293:2001–2006,
C 2010 Wiley-Liss, Inc.
2010. V
Key words: Eublepharis macularius; homology; circumorbital
bones; postfrontal; postorbital; postorbitofrontal
Recently Daza and Bauer (2010) reviewed the pattern
and occurrence of the circumorbital series of bones in
Gekkotans, recognizing five nominal elements in this
cluster (prefrontal, postfrontal, postorbital, jugal, and
lacrimal). They noted that in lepidosaurs, this general
pattern of circumorbital elements is variously modified
by integration with the tooth-bearing maxilla and the
longitudinal and dorsally situated frontal and by the
variable presence of neomorphic elements (palpebrals,
supraorbital and parafrontals). Of the circumorbital elements proper, Daza and Bauer (2010) reported that only
the prefrontal is invariable in its participation in the orbital margin.
C 2010 WILEY-LISS, INC.
V
The orbit of gekkotans can be disproportionately large,
when compared with that of other squamates, and it is
always incomplete posteriorly (the outcome of a reduction in relative size and shape of the postorbital and the
*Correspondence to: Patrick Arthur David Wise, Department
of Biological Sciences University of Calgary, 2500 University
Dr. N.W. Calgary, AB Canada T2N 1N4. Fax: 403-289-9311.
E-mail: padwise@ucalgary.ca
Received 6 May 2010; Accepted 26 August 2010
DOI 10.1002/ar.21277
Published online 2 November 2010 in Wiley Online Library
(wileyonlinelibrary.com).
2002
WISE AND RUSSELL
Fig. 1. Schematic representation of element identity and location in
the dorsal circumorbital region of lepidosauromorphs in left lateral
view. Blocks indicate relative placement and proportions, and translucency indicates element overlap. Color coding of elements follows the
convention used by Daza and Bauer (2010): orange, frontal; white, pa-
rietal; yellow, postfrontal; blue, postorbital; green, postorbitofrontal.
Conditions represented: A: basal pattern as seen in Sphenodon; B:
the gekkotan pattern as advocated by Daza and Bauer (2010); C: the
gekkotan pattern as proposed by Evans (2008); D: the pattern displayed by Eublepharis macularius, this study.
jugal) and is confluent with the single opening resulting
from the confluence of the supratemporal and infratemporal fenestrae. These traits have resulted in major
changes in both the configuration and presence of elements of the circumorbital series.
Daza and Bauer (2010) not only paid particular attention to the determination of the presence of the lacrimal
and jugal in gekkotans but also commented on the prefrontal and the putatively combined postfrontal and
postorbital, which they argued is primitively present in
the Gekkota as the postorbitofrontal. It was reported by
Daza and Bauer (2010) that the postfrontal and postorbital apparently fuse to form a single element in some
members of all lizard clades (Fig. 1B), a tendency also
noted by Conrad (2008). This differs from the primitive
situation in which a separate postfrontal and postorbital
occur in the dorsal rim of the orbit (Fig. 1A). In the latter case the postfrontal contacts the frontal and parietal
and bridges the suture between these bones, and the
postorbital contacts the postfrontal but is excluded from
contact with the frontal and parietal by the intervening
postfrontal (consistent with the condition figured for
Elgaria coerulea by Maisano, 2001). Daza and Bauer’s
(2010) conclusion about the identity of the single element
that subtends and spans the frontoparietal suture in the
dorsal rim of the orbit was that it is the result of such
fusion (Daza and Bauer, 2010), in accordance with an earlier proposal of Daza et al. (2008). They identified this
putatively combined element as the postorbitofrontal,
adopting the most conservative interpretation because it
does not necessitate the loss of either element. Their
interpretation was guided primarily by the observation
that basal members of the Gekkonomorpha posses both
elements (Conrad and Norell, 2006), and additionally on
statements such as that of Siebenrock (1895) that the
postorbital is absorbed by the postfrontal. Empirical evidence for such fusion is, however, rather slender.
Daza and Bauer (2010) surveyed 105 species of gekkotans and reported a single element lying at the posterodorsal corner of the orbit, clasping the frontoparietal
suture, in all species except Lygodactylus that they
examined. This element is usually triangular in outline,
with a laterally oriented vertex, but some taxa depart in
modest ways from this general configuration. Contact of
this element with the prefrontal occurs only in Phelsuma. In some pygopodids, this putative postorbitofron-
tal is perforated by one or two foramina (Stephenson,
1962; Kluge, 1976).
Evans (2008) had previously postulated that the single
ossification bridging the frontoparietal suture in limbed
gekkotans is the postfrontal (Fig. 1C). This accords with
the interpretation given by El-Toubi and Kamal (1961),
who posited that the postorbital is absent. Evans (2008)
indicated that there is a compound bone only in pygopodids that results from fusion of the postfrontal and
postorbital (Fig. 1B). This would imply the absence of
postorbital in limbed gekkotans. Reasons for interpretation of Evans (2008) were that two bones are present in
this location in one species of the pygopodid genus Lialis, as reported by Rieppel (1984), and that the presence
of one or more perforations in the single element found
in some species of Delma, Lialis, and Pygopus belies evidence of fusion only in the pygopods. However, Daza and
Bauer (2010) argued that because pygopodids are nested
within limbed gekkotans, the likely primitive state for
the Gekkota in its entirety is the presence of a fused
postfrontal and postorbital, resulting in the presence of
a postorbitofrontal (Fig. 1B).
However, there is no direct developmental evidence
available for the testing of these two competing hypotheses, each of which is based on extrapolation from
observed adult morphology that is interpreted in different ways in a broader systematic context. Evans’ (2008)
hypothesis leads to the prediction that in development
only a postfrontal element (Fig. 1C), represented by a single center of ossification, should appear in limbed gekkotans and that either there should be no evidence of the
presence of a postorbital or that the latter will make only
a transient appearance and then degenerate. Conversely,
the hypothesis of Daza and Bauer (2010) leads to the prediction that in all gekkotans ossification centers for the
postfrontal and postorbital should occur, with these centers later coalescing into a single unit. In both instances,
the outcome will yield a single element that bridges the
suture between the frontal and the parietal, with the contact being made either by the postfrontal alone or by the
base of the postfrontal to which the postorbital has
become fused in a lateral location, not likely participating
in the contact with the frontal and parietal.
Our investigation of the sequence and pattern of ossification of cranial elements in the eublepharid gekkotan
Eublepharis macularius enables us to report on
EUBLEPHARIS
2003
CIRCUMORBITAL BONES
Fig. 2. The right postorbital of Eublepharis macularius in dorsolateral view, from the initiation of ossification in Stage 35 (A), through Stages 36 (B), 37 (C), 38 (D–F), 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.
ossification events in the dorsal circumorbital region at
a critical juncture in development and allows us to
address the predictions consistent with the hypotheses
of Evans (2008) and Daza and Bauer (2010).
MATERIALS AND METHODS
Our data are based on 32 embryos that encompass developmental Stages 34–42 (Wise et al., 2009) of the Leopard gecko (Eublepharis macularius). These embryos were
cleared and stained using methods modified from those of
Filipski and Wilson (1985), staining only with Alizarin red
S (to enable detection of ossification centers in dermal elements and the tracing of their development through subsequent stages). An additional series of double-stained
embryos was prepared, so we are able to confirm that none
of the elements reported here display any presence of cartilage or its precursors. All elements were initially examined in situ. However, for detailed examination of the
skeletal structures in question, the head skeleton of each
embryo was gently teased apart to isolate individual elements, permitting an unobstructed view of their anatomy.
Observations were made using a Nikon SZ800 dissecting microscope. Images were taken using a Nikon D200
Camera and were cropped and sized in Adobe Photoshop
Version 9.0.2. Additionally, the images were refined using
the sharpen filter and auto levels commands in Photoshop.
RESULTS
An ossification center occupying the classical position
of a postfrontal (Fig. 1A) (Conrad, 2008; Daza and
Bauer, 2010) first 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. 2D–F), 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 ossification
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 definitive
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 ossification center that occupies a
position anterior to the triangular element lying
2004
WISE AND RUSSELL
alongside the frontal as described above. This, however,
only has a transient independent existence. It is first
observed late in Stage 36 (Fig. 3A) as a thin splint lying
lateral to the dorsolateral edge of the bridge of the frontals. By early Stage 38 (Fig. 3B), this element is still separated largely from the frontal, but by mid-Stage 38 (Fig.
3C), its caudal end is extensively ossified and is connected to the dorsolateral edge of the frontal, although its
midsection and rostral end still remain free. From the
dorsolateral edge of the caudal end of the frontal, a progressive expansion of ossification begins that extends
anteriorly to meet the caudal end of the lateral splint.
The dorsolateral edge of the caudal end of the frontal
takes the form of the barb of a fish-hook. Throughout
these developmental stages, elongation of the supraorbital splint continues, so that by Stage 39, it excludes the
frontal from the orbital margin and now comes to lie
between the prefrontal and the frontal as well as between
the triangular element described above, and the frontal
(Fig. 3D). Coalescence continues, progressing from caudal
to rostral, resulting in the fusion of the supraorbital
splint to the dorsolateral edge of the frontal. By Stage 39
(Fig. 3D), fusion to the frontal is almost complete, except
for the rostralmost portion. The prior presence of the
once-independent splint is still evident, however, as a
thin strut along the dorsolateral edge of the frontal. By
Stage 40, complete fusion between the splint and the
frontal has occurred (Fig. 3E).
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 roofing
bones, namely the frontal and the parietal.
Predictions resulting from Daza and Bauer’s (2010)
hypothesis indicate that ossification centers for the postfrontal and postorbital should both appear and then
should fuse to form a composite postorbitofrontal. Again
these are partially borne out. Two elements do appear
(Figs. 2 and 3), but they do not fuse to each other, and
they do not exhibit the primitive relationship of the postorbital to the postfrontal (Fig. 1A), but rather lie in series. The splint-like element unites with the frontal (Fig.
3), and the triangular element persists as a robust independent bone, clasping the frontoparietal suture as well
as fulfilling all of the criteria for recognition as the postfrontal (Fig. 2), if it was present alone, rather than fused
postorbitofrontal.
Our results cannot fully resolve the competing hypothesis as they relate to the Gekkota in its entirety because the
Eublepharidae is the sister taxon to Sphaerodactylidae þ
[Gekkonidae þ Phyllodactylidae], whereas the Diplodactylidae þ [Carphodactylidae þ Pygopodidae] constitutes the
sister taxon to that cluster (Gamble et al., 2008). Thus, the
condition advocated for the pygopods of a fused postfrontal
and postorbital could still pertain and could also be a characteristic of the Diplodactylidae and the Carphodactylidae.
However, the eublepharids are basal to the sphaerodactylids, gekkonids, and phyllodactylids (Daza and Bauer,
2010: Fig. 2) and, thus, can be hypothesized to exhibit a
condition characteristic of this cluster, especially as it
appears to represent a situation somewhat similar to that
of basal lepidosauromorphs (Daza and Bauer, 2010: Figs.
1A,2) and some primitive gekkonomorphs (Conrad and
Norell, 2006), with the exception that the anterior element
is fused to the frontal rather than being free, a condition
also noted to occur in some iguanids (Norell, 1989). Eublepharids retain many primitive features among gekkotans
(Kluge, 1962; Daza, personal communication); thus the
dorsal circumorbital bones could represent another example of such expression. The developmental pattern exhibited by Eublepharis, however, places in doubt the validity
of transferring the trait of a compound postorbitofrontal to
encompass all of the Gekkota (Daza and Bauer, 2010).
As a result of our observations, three alternative
hypotheses can be erected. The first posits that both the
postfrontal and postorbital elements are present but
their anatomical relationships have changed, the postfrontal undergoing reduction in size and an anterior
shift to lie alongside the frontal and to contact the prefrontal, with the postorbital being retained (as per Rieppel, 1992) and extending medially to contact the
frontoparietal suture (Fig. 1D). Because this necessitates
the recognition of no additional elements, and because
we found no evidence of fusion between developmental
centers representing the postfrontal and postorbital, we
favor this interpretation.
Alternatively the splint-like element that abuts, and
later fuses with, the frontal could represent a de novo
ossification that has no homolog in other squamates.
This would then leave the triangular element to be identified as the postfrontal (because of its anatomical relationships) and the postorbital would be absent.
The third alternative would be to recognize the splintlike element that fuses with the frontal as a de novo element and the triangular element that articulates with
the frontal and parietal as a combined postorbitofrontal
(Fig. 1B, in part), but there is no developmental evidence to support this.
Thus, our preferred interpretation (Fig. 1D) requires
only a shift in position of elements already known to be
present primitively in the Squamata (Indeed, this could
Fig. 3. The postfrontal of E. macularius from (A) initiation of ossification in late Stage 36 to complete fusion with the frontal (E) in Stage
40 (staging according to Wise et al., 2009). Panels A–C are in dorsolateral view; D and E are dorsal views, and rostral is to the right in all
views. A–C 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 A–D 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
WISE AND RUSSELL
also be interpreted as the retention of the primitive location of the postfrontal and an anterior shift of the postorbital—the 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 ossification (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 five developmental stages (range, 36–40) over
which the initiation of ossification of the postfrontal (our
preferred interpretation—see 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 ossification 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.
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