An Osteological and Histological Investigation of Cranial Joints in Geckos

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1 THE ANATOMICAL RECORD 294: (2011) An Osteological and Histological Investigation of Cranial Joints in Geckos SAMANTHA L. PAYNE, 1 * CASEY M. HOLLIDAY, 2 AND MATTHEW K. VICKARYOUS 1 1 Department of Biomedical Sciences, University of Guelph, Guelph, Ontario, N1G 2W1, Canada 2 Department of Pathology and Anatomical Sciences, University of Missouri, Columbia, Missouri ABSTRACT Cranial kinesis is a widespread feature of gekkotan lizards. Previous studies of kinesis in lizards often described the relevant, mobile joints as synovial, thus characterized by the presence of a synovial cavity lined with articular cartilage. To date however, detailed investigations of cranial joint histology are lacking. We examined eight cranial joints (quadrate articular, quadrate pterygoid, quadrate otooccipital, quadrate squamosal, epipterygoid prootic, epipterygoid pterygoid, basisphenoid pterygoid, and frontal parietal) in five gekkotan species (Oedura lesueuerii, Eublepharis macularius, Hemitheconyx caudicinctus, Tarentola annularis, and Chondrodactylous bibronii) using microcomputed tomography and serial histology. Particular focus was given to the relationship between the bony and soft-tissue components of the joint. Our results demonstrate that only three of these joints are synovial: the quadrate articular, epipterygoid pterygoid, and basisphenoid pterygoid joints. The frontal parietal and quadrate pterygoid joints are syndesmosis (fibrous), the epipterygoid prootic and quadrate otooccipital joints are synchondroses (cartilaginous without a synovial cavity) and the quadrate squamosal joint was not present. Based on previous descriptions, we determine that the structure of some cranial joints is variable among lizard taxa. We caution that osteology does not necessarily predict cranial joint histology. Although the functional implications of these findings remain to be explored we note that the development of synovial joints appears to be associated with a neural crest origin for the elements involved. Anat Rec, 294: , VC 2011 Wiley-Liss, Inc. Key words: cranial kinesis; synovial joint; quadrate; gekkota; microcomputed tomography; histology INTRODUCTION Among modern squamates, cranial kinesis, or intracranial movement, is typically associated with the evolution of temporal fenestration, a reduction in the size and/or robusticity of individual skull elements and the functional integration of a series of moveable joints (Schwenk, 2000). These moveable joints include diarthroses (synovial joints) and several structural forms of synarthroses. Anatomically, a synovial joint is characterized by the presence of articular cartilage (hyaline-like cartilage lacking a perichondrium), a fluid-filled synovial cavity and a joint capsule (Barnett, 1961; Archer et al., Grant sponsor: Natural Sciences and Engineering Research Council Discovery Grant (to MKV); Grant number: ; Grant sponsor: NASA Space Grant Consortium Research Initiation Award (to CMH). *Correspondence to: Samantha L. Payne, Department of Biomedical Sciences, University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1 Canada. spayne@uoguelph.ca Received 13 September 2010; Accepted 15 November 2010 DOI /ar Published online 19 January 2011 in Wiley Online Library (wileyonlinelibrary.com). VC 2011 WILEY-LISS, INC.

2 400 PAYNE ET AL. TABLE 1. Summary of cranial joints in structural-grade lizards Agamidae Iguanidae Teiidae Cordylidae Varanidae Gekkota Phelsuma madagascariensis (Herrel et al., 1999) This Study Gekko gecko (Herrel et al., 1999) Afroedura karrocia (Webb, 1951) Palmatogecko rangei (Webb, 1951) Varanus bengalensis (Rieppel, 1978) Cordylus polyzonus (Van Pletzen, 1946) Tupinambis nigropunctatus (Jollie, 1960) Iguana iguana (Throckmorton, 1976) Ctenosaura pectinata (Oelrich, 1956) Uromastyx aegyptius (Throckmorton, 1976) Synovial Synovial Synovial Synovial Synovial Synovial ND ND ND ND Synovial Syndesmosis Syndesmosis Syndesmosis Syndesmosis Syndesmosis Syndesmosis Syndesmosis ND Synovial and syndesmosis Synovial and syndesmosis Synovial and syndesmosis ND ND ND ND Synovial Synovial Syndesmosis Syndesmosis Synchondrosis Synchondrosis Synchondrosis ND ND Synchondrosis Synchondrosis Not present Synchondrosis ND Synchondrosis ND ND Ligamentous attachment ND ND ND ND Syndesmosis Syndesmosis Syndesmosis Syndesmosis ND ND Synchondrosis ND ND ND Synovial Synovial Synovial Synovial Synovial ND ND Synovial Quadratearticular Quadratepterygoid Quadrateotooccipital Quadratesquamosal Epipterygoidprootic Epipterygoidpterygoid Basisphenoidpterygoid ND ND ND ND ND Synovial Synovial Synovial ND ND Synovial Frontal-parietal ND ND ND Syndesmosis ND Syndesmosis Syndesmosis Syndesmosis ND ND Syndesmosis ND, no data. 2003). The joint capsule includes a smooth synovial membrane surrounded by multiple layers of dense fibrous tissue. All nonsynovial joints (i.e., lacking articular cartilage, a synovial cavity and a joint capsule) are synarthroses. Synarthroses include essentially immobile bone-to-bone synostoses (sutures), synchondroses (characterized by an intervening cartilage segment), and syndesmosis (fibrous tissue-based connections; Barnett, 1961). Two principle types of cranial kinesis can be demonstrated by squamates: streptostyly and mesokinesis. A third controversial type of movement, metakinesis, is frequently reported (e.g., Smith, 1980; Schwenk, 2000) but has yet to be conclusively demonstrated (Metzger, 2002; Johnston, 2010). Each category of kinesis is defined by a characteristic cranial movement involving a series of interdependent joints. For example, streptostyly is typically summarized as rotation of the quadrate bone on the braincase (Herrel et al., 1999; Metzger, 2002). Hence, each articulation of the quadrate must allow for mobility. This includes movement of the quadrate at the otooccipital (exoccipital þ opisthotic) region of the braincase (Metzger, 2002; Evans, 2009), the pterygoid bone of the palate, the articular bone of the mandible and, in some taxa, the squamosal bone at the caudolateral margin of the skull (Throckmorton, 1976; Herrel et al., 1999; Metzger, 2002). Furthermore, displacement of the quadrate during streptostyly is often associated with some combination of mesokinesis, dorsoventral flexion of the frontal parietal joint, and possibly metakinesis, movement between the dermatocranium and braincase (Evans, 2009). Combined, these actions are facilitated by articulations between the braincase and epipterygoid, epipterygoid and pterygoid, and basipterygoid and pterygoid (Frazzetta, 1962; Metzger, 2002; Evans, 2009). Notwithstanding the importance of moveable joints to cranial kinesis, histological details of joint anatomy remain limited (Metzger, 2002; see Table 1) and the relationship between structure and function unclear. The aim of this study is to investigate the osteology and histology of cranial joints in five representative geckos, with a particular focus on the quadrate articular, quadrate pterygoid, quadrate otooccipital, quadrate squamosal, epipterygoid prootic, basisphenoid pterygoid, epipterygoid pterygoid, and frontal parietal articulations. We combine microcomputed tomography (lct) and serial histology to document the skeletal morphology and soft tissue structure of these joints. Geckos are of particular relevance to cranial kinesis because they are one of the few lepidosaur clades to clearly demonstrate the phenomenon (Herrel et al., 1999). Moreover they are consistently found to be the most primitive clade of living squamates (Townsend et al., 2004; Vidal and Hedges, 2005), making their structural and functional adaptations important to understanding the evolution of kinesis among lizards as a group. MATERIALS AND METHODS Micro-Computed Tomography (lct) Imaging Osteological descriptions are based on lct scans of adult-sized formalin fixed, alcohol stored specimens. Gekkotans investigated include a single specimen of each of the diplodactylid Oedura lesueurii (Lesueur s velvet gecko), the eublepharids Eublepharis macularius

3 GECKO CRANIAL JOINTS 401 ar bs ep fb fr hc ot po pr pt q sc sq TABLE 2. Anatomical abbreviations articular basisphenoid epipterygoid fibrous tissue frontal hyaline cartilage otooccipital prootic parietal pterygoid quadrate synovial cavity squamosal (leopard gecko), and Hemitheconyx caudicinctus (African fat tailed gecko), the phyllodactylid Tarentola annularis (white-spotted gecko) and the gekkonid Chondrodactylous bibronii (Bibron s gecko). Scans were conducted using either a GE Medical Systems model R59-80, 1600 watts, single phase lct scanner (Comparative Orthopedic Research Group, University of Guelph, Ontario, Canada: E. macularius, T. annularis, C. bibronii; 80 kv, 450 ma, interslice spacing: lm) or a GE explore Locus in vivo Small Animal lct scanner (Ohio University, Athens, Ohio: O. lesueurii, H. caudicinctus; 70 kv, 400 ma, interslice spacing: 92 lm). Datasets were rendered in three-dimensions using Amira Histological Sectioning and Staining Following lct scanning, each gecko head was prepared for serial sectioning. E. macularius, T. annularis, and C. bibronii were investigated using paraffin sections as follows: tissue was first decalcified using Cal-ExVR (Fisher Scientific) for 45 min, dehydration to 100% ethanol, cleared in xylene and then embedded in paraffin wax (Fisher Scientific). Sections were cut at 5 lm ona rotary microtome and mounted on charged slides (Snow Coat X-tra, Surgipath). Following histochemical staining (see below), sections were mounted with cryoseal (Fisher Scientific). Paraffin-embedded tissues were stained using a modified Masson s trichrome (Witten and Hall 2003). Sections were then dehydrated in an alcohol series and coverslipped. O. lesueurii and H. caudicinctus were investigated using plastic sections as follows: Specimens were stored in 95% and then 70% ethanol (due to infused fluorochrome bone labels), dehydrated with graded solutions of ethanol, and cleared with xylenes in preparation for resin infiltration with methyl methacrylate (MMA) and dibutyl phthalate (DBP). Specimens were then embedded in a fresh solution of MMA, DBP, and Perkadox-16 and allowed to polymerize using a combination of room temperature, refrigeration, a waterbath, and an oven over the course of two weeks (additional details in Holliday et al., 2010). Using the Donath-Technique (Donath, 1995) and the EXAKT Cutting and Grinding System (EXAKT Technologies, Oklahoma City, OK), micron slide mounted serial sections were cut, ground, and polished to a final thickness of microns. Slides were stained using Sanderson s Rapid Bone Stain (Dorn and Hart Microedge, Villa Park, IL) alone and in Fig. 1. Three-dimensional microcomputed reconstruction of the skull of Eublepharis macularius, a representative gekkotan. (A) Skull in oblique dorsolateral view. (B) Close-up view of the cephalic condyle of the quadrate and adjacent otooccipital and squamosal elements in lateral view. combination with Van Gieson s Picrofuchsin as a counterstain. The anatomical terminology used follows the work of Daza et al., (2008). Abbreviations can be found in Table 2. RESULTS Here the structure of cranial joints involved in cranial kinesis was investigated using lct, serial histology and histochemistry. Detailed descriptions of gekkotan osteology are available elsewhere (e.g., Wellborn, 1933; Jollie, 1960; Kluge, 1962; Daza et al., 2008; Evans, 2009). With respect to the features relevant to this investigation, the skull is broadly similar (Fig. 1), and unless otherwise noted descriptions apply to all five taxa. The quadrate is the elongate bone located caudal to the orbit and immediately rostral to the middle ear cavity (Fig. 1A). The quadrate links the mandible with braincase (otooccipital) and serves as the cranial attachment of m. adductor mandibulae posterior (Haas, 1973; Daza et al., 2008). When in a neutral position, l-ct imaging of Eublepharis reveals the long axis of the quadrate has a near vertical orientation. In caudal view the quadrate has a blade-like appearance (comparatively wider dorsally than ventrally) with distinctive cephalic and mandibular condyles, each capped with cartilage. The caudal surface of the element is concave where it is excavated by the middle ear cavity. The mandibular condyle articulates with the articular surface of the articular bone and has a smooth bicondylar surface capped with articular cartilage (Fig. 2A). The articular surface of the mandible is reciprocally shaped, with a raised saddle-like articulation surface. Similar to the mandibular condyle, the articular bone is superficially capped with a layer of articular cartilage. Although the mandibular condyle and articular surface are separated by a narrow cavity, the two are firmly linked to one another by thick, fibrous tissue capsule (Fig. 2B). The medial portion of the ventral quadrate articulates rostrally with the pterygoid bone of the palate (Fig. 2C). In transverse section this articulation is marked by a shallow concavity. Neither the quadrate process of the pterygoid nor the receiving facet of the quadrate

4 402 PAYNE ET AL. Fig. 2. Osteology and histology of cranial joints in gekkotans. Three-dimensional microcomputed (lct) reconstructions of the quadrate-associated joints investigated (A,C,E,G) paired with corresponding histological sections (B,D,F,H). All lct reconstructions are taken from the E. macularius model. Serial section (H) is plastic embedded and stained with toluidine blue and picrofuchsin; all others are paraffin-embedded and stained with Masson s Trichrome. Yellow lines indicate from which plane of section the joint was sampled. (A) Rostral view of the quadratearticular joint. (B) Histological section of the same specimen as (A) taken transversely through the quadrate articular articulation. The presence of a synovial cavity, articular cartilage, and fibrous capsule are indicative of a synovial joint. (C) Caudal view of quadrate pterygoid articulation. (D) Transverse section of the quadrate pterygoid joint of Tarentola annularis. Fibrous tissue rather than cartilage is present on articulating surfaces, indicative of a syndesmosis. (E) Lateral view of the quadrate otooccipital joint. (F) Transverse section of the quadrate otooccipital joint of Chondrodacylus bibronii. This joint involves hyaline cartilage (on the quadrate) and dense fibrous tissue, characteristic of a synchondrosis. (G) Lateral view of the quadrate squamosal joint. (H) Transverse view of the quadrate squamosal joint of Oedura lesueuerii. The quadrate and squamosal are separated by muscle tissue and do not articulate in any of the species investigated. Scale bars = 1 mm. develops cartilage. The intervening cavity between the two elements (Fig. 2D) is reinforced by loose irregular and dense regular fibrous connective tissue that spans the elements, is continuous with surrounding periosteum and is deeply embedded into the two elements via Sharpey s fibers The rounded, unicondylar cephalic process of the quadrate articulates with the lateral surface of otooccipital: the fused opisthotic and exooccipital units of the basicranium (Stephenson, 1960; Daza et al., 2008; Fig. 2E). The cephalic condyle of the quadrate is capped with hyaline cartilage, but unlike the quadrate articular joint there is no intervening cavity. Instead, hyaline cartilage of the cephalic condyle grades into fibrocartilage as it approaches the contact with the otooccipital bone. This fibrocartilaginous connection with the otooccipital is reinforced with dense regular fibrous tissue (Fig. 2F). The quadrate does not directly articulate with the squamosal in any of the taxa sampled (Figs. 1B, 2G). Instead the space between the two elements is filled with a portion of m. adductor mandibulae externus superficialis and fibrous connective tissue (Fig. 2H). The epipterygoid is a gracile, columnar bone situated caudal to the orbit in a nearly vertical orientation, roughly parallel with the quadrate (Fig. 1A). As a derivative of the palatoquadrate, the epipterygoid provides a direct linkage between the pterygoid ventrally (Fig. 3E) and the crista alaris of the prootic bone dorsally (Fig. 3A; Daza et al., 2008). Each of the dorsal and ventral articular surfaces is comparatively blunt and capped with cartilage. Although the dorsal head of the epipterygoid is capped by a thin layer of hyaline cartilage, there is no evidence of a synovial cavity between the two elements, rather they are united by dense regular connective tissue fibers (Fig. 3B). The ventral head of the epipterygoid articulates with the dorsal surface of the pterygoid within the rounded fossa columella (Daza et al., 2008; Fig. 3E). In section, both the condyle of the epipterygoid and the fossa columella of the pterygoid are lined with articular cartilage and separated by a fibrous tissue lined cavity (Fig. 3F). The fibrous capsule surrounding the joint is thickened on its lateral margin, where it attaches to pterygoid. Ventromedial to the epipterygoid pterygoid articulation, the pterygoid contacts the braincase via the basipterygoid process of the basisphenoid. The basipterygoid process is capped by a long, wedge-shaped cartilaginous process which abuts the pterygoid meniscus, a cartilaginous cap associated with the dorsal surface of the pterygoid. The two cartilaginous processes lie within a cavity surrounded by a joint capsule composed of fibrous connective tissue. The frontal and parietal bones are both flat, thin elements that contribute to the skull roof, spanning from

5 GECKO CRANIAL JOINTS 403 Fig. 3. Osteology and histology of cranial joints in gekkotans. Three-dimensional microcomputed (#CT) reconstructions of the joints investigated (A,C,E,G) paired with corresponding histological sections (B,D,F,H). All #CT reconstructions are taken from the E. macularius model. Serial section (B) is plastic embedded and stained with toluidine blue and picrofuchsin; all others are paraffin-embedded and stained with Masson s Trichrome. Yellow lines indicate from which plane of section the joint was sampled (A) Lateral view of epipterygoid prootic joint. (B) Sagittal section of the epipterygoid prootic joint of Hemitheconyx caudicinctus. The epipterygoid is capped with hyaline cartilage and the two elements are joined by fibrous tissue consistent with a synchondrosis. (C) Dorsolateral view of the basisphenoid pterygoid joint. (D) Sagittal section of the basisphenoid pterygoid joint of E. macularius. Both elements are capped with cartilage, separated by an intervening synovial cavity and surrounded by fibrous tissue, indicative of a synovial joint. (E) Dorsolateral view of epipterygoid pterygoid joint. (F) Sagittal section of the epipterygoid pterygoid joint of T. annularis. This articulation is defined by a synovial cavity and surrounding fibrous capsule, as well as articular cartilage, consistent with other synovial joints. (G) Dorsal view of frontal parietal joint. (H) Parasagittal section of the frontal parietal joint of E. macularius. The dense organization of fibrous tissue without cartilage indicates a syndesmosis. Scale bar = 1 mm. the nasal bone to the supraoccipital region of the skull (Fig. 1A). The frontals are fused and situated rostrally while the paired parietals occupy a more caudal position. The parietal forms the major portion of the posterior roof of the skull and provides the surface for the attachments of several jaw muscles. Contact between the frontal and parietal occurs across a prominent transverse joint caudal to the orbit (Fig. 3G). This articulation consists of dense connective fibers arranged in parallel (Fig. 3H). There is no evidence of either cartilage or an intervening cavity. DISCUSSION Of the eight cranial joints investigated, two are syndesmosis, two are synchondroses, and three are synovial. All three synovial joints, the quadrate articular, epipterygoid pterygoid, and basisphenoid pterygoid, are highly conserved among lizards, as is the syndesmotic frontal parietal joint (Table 1). The histological structure of the remaining joints is taxonomically variable. For example, the quadrate pterygoid joint is a syndesmosis in gekkotans, the teiid Tupinambis nigropunctatus (Jollie, 1960), and the iguanid Iguana iguana (Throckmorton, 1976). In other lizards (e.g., the iguanid Ctenosaura pectinata; Oelrich, 1956) it is reportedly a composite joint, part synovial, and part syndesmosis. Furthermore, based on the taxa sampled, we identify the quadrate otooccipital articulation as a synchondrosis, matching the structural interpretations of this joint in the gekkotans Gekko gecko and Phelsuma madagascariensis (Herrel et al., 1999). Other investigations have concluded that the quadrate otooccipital is either a syndesmosis (some gekkotans) or a synovial joint (Cordylus polyzonus, Varanus bengalensis) and (at least in V. bengalensis) includes a disc of intercalary cartilage between the two elements. The epipterygoid prootic joint is also variable. We identify it as a synchondrosis whereas in other taxa (including other gekkotans) it has been reported as a syndesmosis (e.g., Van Pletzen, 1946; Webb, 1951). Whereas a contact between the quadrate and squamosal bones has been reported for various squamates, including the gekkotans G. gecko and P. madagascariensis (Jollie, 1960; Rieppel, 1978; Grismer, 1986; Herrel et al., 1999), none of the species investigated herein demonstrated any evidence of a direct connection. Using lct imaging, we observed that the squamosal projects dorsal and caudal to the dorsal condyle of the quadrate (Figs.1B,G). However, serial histology confirms that the two elements do not articulate. Although not the focus of our investigation, it remains possible that the quadrate and squamosal are indirectly connected by ligaments, as has been described for other taxa (Rieppel, 1984). This, however, was not observed in the species studied here.

6 404 PAYNE ET AL. At present, the functional implications of joint histology remain poorly understood in the heads of lepidosaurs and other reptiles. A recent investigation of the basal lepidosaur Sphenodon determined that whereas the cranium is functionally akinetic, the basipterygoid pterygoid (¼ palatobasal) joint remains synovial (Johnston, 2010). Additionally, Holliday and Witmer (2008) demonstrated this joint is also likely synovial among most avian and nonavian archosauriforms, and may even be plesiomorphic for amniotes (see also Iordansky, 2000). A similar situation is observed in crocodyliforms, which maintain functionally immobile synovial joints between the braincase (specifically the laterosphenoid) and postorbital, and the quadrate and otooccipital (Holliday and Witmer, 2009). Consequently, while synovial joints appear to be required for functional cranial kinesis, their presence does not necessarily imply the phenomenon. Gekkotans are streptostylic (Herrel et al., 2000) and have three separate types of articulations facilitating quadrate movement: synovial at the jaw joint (Fig. 2B); syndesmosial with the pterygoid (Fig. 2D), and synchondrosial with the otooccipital (Fig. 2F). Combined, these data reveal that streptostylic displacement is facilitated by a complex linkage of joints with varying structural properties. Interestingly, the histological structure of the joints permitting streptostyly often varies between taxa. For example, unlike gekkotans the dorsal end of the quadrate in varanids contributes to a synovial joint (Rieppel, 1978). This morphological difference between the two joints may be the reason the rostrocaudal displacement of the quadrate during streptostyly is reportedly greater in varanids (27 degrees in V. bengalensis; Rieppel, 1978) than in gekkotans (13.2 degrees in P. madagascariensis, 5.6 degrees in G. gecko; Herrel et al., 2000). In part the differences in tissue structure are likely related to the morphology of the individual elements involved, the integrated effect of multiple linkages and dietary behavior. The age of the specimen may also influence the degree of rotation. Furthermore, the overall pattern and complement of elements involved in cranial kinesis varies among lizard groups (McBrayer and Corbin, 2007), highlighting the importance of avoiding generalizations among taxa. These data establish that osteology is not necessarily an accurate predictor of joint structure and soft tissue composition. For example, rounded condyles are often interpreted as evidence of a synovial joint (Barnett, 1961). Among gekkotans the quadrate bone has distinctive ventral and dorsal condyles (Fig. 1A,B), but only the mandibular condyle contributes to a synovial joint. The cephalic condyle participates in a synchondrosis. Conversely, the epipterygoid lacks well-defined condyles but contributes to both a synovial joint (ventrally with the pterygoid; Fig.3F) and a synchondrosis (dorsally with the prootic; Fig. 3B). Although presently untested, detailed examination of joint structures may reveal that some soft-tissue features leave identifiable osteological correlates (e.g., a rugose joint periphery indicative of the fibrous capsule attachment; see Holliday and Witmer, 2008). Until such time, we conclude that the interpretation of joint structure from osteological correlates must be approached with caution. Skeletal development may present a further complication in evaluating joint structure, particularly in the absence of serial histology. For example, both the quadrate and epipterygoid are replacement elements that initially develop as cartilaginous models (Evans, 2009). In some species (e.g., Lacerta agilis exigua) these elements are fully ossified in hatchlings (Rieppel, 1994), whereas in others they are not (Maisano, 2001; Evans, 2009). Hence the presence of cartilage associated with these elements, even post-hatching, may represent incomplete skeletal development. These observations may explain the structural variation reported for the epipterygoid prootic joint (Table 1). It should also be noted that oviparous species are more skeletally mature (i.e., more fully ossified) at hatching than comparably aged viviparous taxa (Maisano, 2001), and cranial kinetic movements appear to diminish with age in squamates (Metzger, 2002). Taken together, we suggest that the relative age of the individual represents an important but often neglected variable in the interpretation of joint structure and function. Lastly, we note that joint structure may reflect the developmental origin of the elements involved. Among birds and mammals, neural crest cells give rise to the articular, quadrate, epipterygoid, pterygoid, and at least a portion of the frontal bone (Noden and Trainor, 2005) and basisphenoid (McBratney-Owen et al., 2008). The otooccipital, parietal, prootic, and sometimes a portion of the frontal bone are mesodermal in origin. We observe that craniofacial joints between neural crest derived elements are either synovial or syndesmosial joints, or sutures. In contrast, articulations involving one or more mesodermally derived elements are either syndesmosis or synchondroses. We hypothesize that in the skull, the neural crest is a requirement for a synovial joint formation. ACKNOWLEDGMENTS We thank Mark Hurtig and Karen Lowerson of the Comparative Orthopaedic Research Group (University of Guelph, Canada) for the use of and help with lct imaging; Carol Armstrong for her advice and use of the Axio camera; Helen Coates for her invaluable help with paraffin-embedded histochemical protocols and the microtome; Jack Ratliff for help with plastic-embedded histological methods; Jeff Thomason for his advice on the functional aspect of joint studies; Katie McLean and Stephanie Delorme for their advice and support. LITERATURE CITED Archer CW, Dowthwaite GP, Francis-West P Development of synovial joints. Birth Defects Res C 69: Barnett CH Synovial Joints. London: William Clowes and Sons. Daza JD, Abdala V, Thomas R, Bauer AM Skull anatomy of the miniaturized gecko Sphaerodactylus roosevelti (Squamata: Gekkota). J Morphol 269: Donath K Preparation of histologic sections. Norderstedt: EXAKT-Kulzer Publication. p 16. Evans SE The skull of lizards and Tuatara. 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