Variation in the Position of the Jugal Medial Ridge Among Lizards (Reptilia: Squamata): Its Functional and Taxonomic Significance
Senckenberg Research Institute and Natural History Museum Frankfurt, Palaeoanthropology and Messel Research, Frankfurt am Main, Germany
Geological Institute, Slovak Academy of Sciences, Banská Bystrica, Slovak Republic
Correspondence to: Andrej Čerňanský, Senckenberg Research Institute and Natural History Museum Frankfurt, Palaeoanthropology and Messel Research, Senckenberganlage 25, 60325 Frankfurt am Main, Germany. E-mail: email@example.com
Lizards, together with snakes and amphisbaenians, constitute the Squamata, the largest and most diverse group of living non-avian reptiles (Evans, 2003). Squamates are distributed on every continent except Antarctica, and they evince diverse ecologies and body forms, from limbless burrowers to arboreal gliders (e.g., Greene, 1997; Pianka and Vitt, 2003). Their morphology and relationships have been extensively studied, because major animal adaptations often characterize broad taxonomic groupings (Frazzetta, 1975). This study deals with differences among lizards in the course of the medial ridge located on the jugal's medial aspect. The jugal is a skull bone forming the posterior, ventral and in some taxa even the anteroventral border of the orbit (Romer, 1956; Estes et al., 1988). This bone is present in most vertebrates. It is connected to the quadratojugal and maxilla, and also other bones depending on species. Although numerous past studies have centered on lizard osteology, and many of these provide data on jugal comparative morphology (Estes et al., 1988; Conrad, 2008; Gauthier et al., 2012), differences in the course of the internal medial ridge along the jugal length have largely been overlooked. While Bhullar (2011) described differences in the course of the ridge in Xenosaurus, anatomical comparisons with other groups present a gap in our knowledge.
Morphological features provide evidence on the phylogenetic relationships of the taxa bearing them, and new characters are particularly important in groups where phylogenetic topology is not settled. For squamates, there are stark conflicts between phylogenetic results from morphological and molecular data sets (see e.g., Losos et al., 2012), which are apparent on smaller and larger scales. According to analyses of molecular data, Anguimorpha is divided into two clades, which Vidal and Hedges (2009) named Neoanguimorpha and Palaeoanguimorpha. Neoanguimorpha includes the traditional Anguidae, Heloderma and Xenosaurus, whereas Paleoanguimorpha includes Shinisaurus, Lanthanotus and Varanus (Townsend et al., 2004; Hedges and Vidal, 2009; Vidal and Hedges, 2009; Wiens et al., 2012; Pyron et al., 2013).
Modern analyses of morphological data-sets have never supported this topology but instead universally support the clade Varanoidea, comprising the extant taxa Heloderma, Lanthanotus, and Varanus (Pregill et al., 1986; Estes et al., 1988; Gao and Norell, 1998; Conrad, 2008; Gauthier et al., 2012). Historically, however, a taxonomic division similar to that revealed in molecular phylogenies was occasionally proposed by several authors, using (generally plesiomorphic) morphological characters. Cope (1864) and Boulenger (1884) broke with past classifications in emphasizing osteology and tongue morphology. Boulenger (1884: p 117) was particularly impressed by the osteodermal characters, regarding them as confirming those of osteology and the tongue. Boulenger, like Cope, regarded Helodermatidae as having the greatest “affinity” to Anguidae. Fürbringer (1900) united the following taxa in his Diploglossa or “Anguimorpha”: Anguidae, Heloderma, Xenosaurus and Zonuridae [presumably, following Boulenger 1884, Platysaurus, Chamaesaura, and Zonurus (=Cordylus and relatives)]. He founded this group on the following characters: medial end of clavicle only slightly expanded or not at all, a cruciform interclavicle or one transitional to T-shaped (i.e., with a reduced anterior process), and a papillose tongue. These characters, however, are probably plesiomorphic or shared with other squamate groups. Later, Camp (1923) assigned Helodermatidae, Anniellidae, Anguidae, and Xenosauridae to one clade, which he called Anguioidea; he found the occurrence of a novel superficial muscle of the throat, m. geniomyoideus, to be a compelling feature in support of this group. Camp (1923) regarded this muscle, a special modification of m. genioglossus (Haas, 1973) or m. intermandibularis (McDowell, 1972) that appears to have been overlooked by Zavattari (1910, 1911), to be a novel, or “neotelic,” character, which would be called “apomorphic” in modern terminology. Although he considered Lanthanotus to be a helodermatid (p. 334), he did not dissect it; moreover, he could not have studied Shinisaurus, which was first described in 1930 by Ahl. Haas (1960) later showed that a superficially located m. geniomyoideus is present in Shinisaurus. McDowell (1972; see also Sondhi, 1958) then identified m. geniomyoideus in Varanus, but noted that its position was deep rather than superficial, as in most other anguimorphs. McDowell (1972) and Rieppel (1980) identified a superficial m. genioglossus in Lanthanotus. Given the phylogenetic position assumed by Camp for Lanthanotus, it is unlikely that he would have altered his opinion with regard to the diagnostic characters of his Anguioidea. However, given a sister-group relationship between Varanus and Lanthanotus, the muscle now appears to be a synapomorphy of Anguimorpha, with transformation to a deep position in Varanus, and provides no morphological support for Neoanguimorpha.
Given the want of morphological support for Neoanguimorpha, new anatomical data are essential. The jugal has proven to be of interest for the purposes of identification even of isolated fossil material, and we focus on it here. The aims of this article are: (1) to explore variation in the course of the medial ridge on the jugal's medial aspect, (2) to examine its distribution among lizard taxa; and (3) to establish the causes of variation.
MATERIAL AND METHODS
The following specimens of extant lizard species, plus the Sphenodon outgroup, are used for comparison: Sphenodontidae: Sphenodon punctatus (SMF 7426); Lacertidae: Lacerta viridis (DE 51, SMF 84623 and 33207), L. agilis (DE 78–79, SMF 49552, 49555, 49554, and 49557), Timon pater (SMF 33208), Zootoca vivipara (SMF 49560 and 49561), Podarcis siculus (SMF 50084, 50501, 50080, 50069, and 50086), P. muralis (SMF 12477, 50060, 44976, 49566, 49570, 50059, and 49584); Teiidae: Dicrodon gutulatum (UF 48447), Tupinambis teguixin (SMF 69852, 33242); Gymnophthalmidae: Neusticurus bicarinatus (UF 54554); Scincidae: Tiliqua scincoides (A.Č. personal collection), Plestiodon fasciatus (CM 38472); Agamidae: Hydrosaurus amboinensis (SMF 70930), Agama mossambica (UF 55339), Acanthosaura armata (UF 69015), Uromastyx acanthinura (UF 54136); Polychrotidae: Anolis ricordi (UF 99672), A. garmani (UF 42404), A. barbatus (SMF 79164), Polychrus gutturosus (UF 49377); Corytophanidae: Basiliscus plumifrons (UF 61951); Tropiduridae: Tropidurus torquatus (UF 99338); Iguanidae: Amblyrynchus cristatus (SMF 57458), Dipsosaurus dorsalis (CM 144937); Gerrhosauridae: Gerrhosaurus flavigularis (UF 51543; UF 62345), G. major (CAS 204767), G.(“Angolosaurus”) skoogi (CAS 206978); Cordylidae: Smaug (“Cordylus”) giganteus (SMF 69852 and 69842); Chamaeleonidae: Brookesia brygooi (FMNH 260015), Chamaeleo calyptratus (DE 65, 74–77), Furcifer oustaleti (SMF 59447 and 73685), Trioceros jacksonii (SMF 90037); Helodermatidae: Heloderma suspectum (UF 52265); Xenosauridae: Xenosaurus platyceps (UF 45622, 54911, 54559); Shinisauridae: Shinisaurus crocodilurus (UF 71623); Anguidae: Ophisaurus ventralis (DE 34, 35, 38; AMNH 73057; UF 52539; CM 1411; CM 144985), O. attenuatus (DE 32, 33, 43, 44), Anguis fragilis (DE 14–21, 24, 25, 45–48), Pseudopus apodus (DE 1, 3–13, 22, 23, 29, 52, 54, 58, 59; BSPG 1982 X 2383); Celestus carraui (UF 83555, 83555, 21743, 99990); Barisia rudicollis (DE 69); Mesaspis moreletii (UF 54124) Mesaspis gadovii (UF 62782); Mesaspis monticola (DE 71, 72); Elgaria coerulea (UF 61574); Lanthanotidae: Lanthanotus borneensis (SMF 66188); Anniellidae: Anniella pulchra (UF 51810).
Sphenodon punctatus was used for outgroup comparison. The following specimens of extinct lizard species are also used for comparison: Palaeosaniwa canadensis (MOR 792); Eurheloderma sp. (uncatalogued specimen housed at SMF); Gobiderma pulchrum (IGM 3/55); Exostinus serratus (AMNH 1608); Restes rugosus (YPM 14640), Merkurosaurus ornatus (Pb 01859).
AMNH—American Museum of Natural History, New York, USA.
BSPG—Bayerische Staatssammlung für Paläontologie, Munich, Germany.
DE—Department of Ecology, Comenius University in Bratislava, Slovakia.
NHMUK (BMNH)—Natural History Museum London, United Kingdom.
UF—University of Florida, Gainesville, USA.
CM—Carnegie Museum of Natural History, Pittsburg, USA.
SMF—Senckenberg Research Institute and Natural History Museum in Frankfurt am Main, Germany.
MOR—Museum of Rockies, Montana, USA.
Pb—National Museum, Prague, Czech Republic.
YPM—Yale Peabody Museum of Natural History, USA.
FMNH—Field Museum of Natural History, USA.
CAS—California Academy of Sciences Department of Herpetology, USA.
IGM—Institute of Geology, Ulaan Baatar, Mongolia.
Specimens studied herein were photographed under scanning electron microscopy (SEM) at the Slovak Academy of Sciences and Leica stereomicroscope with digital camera and multifocus Automontage software at the Senckenberg Reasearch Institute.
We do not expect that this one character will alter morphological topologies of Squamata or resolve molecular-morphological conflict. For this reason, we do not conduct a new phylogenetic analysis of Squamata for this article. Instead, our aim is to evaluate whether the distribution of this new character—the position of the medial ridge of the jugal—could support clades previously identified only on the basis of molecular data. To do so, we compiled a metatree in Mesquite that is based on Pyron et al. (2013) for intergeneric relationships, and Townsend and Larson (2002) for chameleon, Bhullar (2011) for xenosaur, Good (1989) and Conrad et al. (2011a) for gerrhonotine, and Stanley et al. (2011) and Bates et al. (2013) for cordyliform relationships. We used Mesquite (Version 2.75.; Maddison and Maddison, 2011) to trace character history using parsimony optimization. (Because information on branch length, such as autapomorphies, was not available for our metatree, parsimony is the only available means of reconstructing character history.)
The absence of members of Gekkota in our study deserves a comment here. Gekkota show reduction of the jugal resulting in an incomplete postorbital bar (see e.g., Estes et al., 1988; Daza and Bauer, 2010). Many members of Varanus also have a reduced jugal (see e.g., Mertens, 1942).
With regard to course of the medial ridge of the jugal, observed variation in lizards may be categorized as follows:
A. The medial ridge is not centrally located:
Type 1. On the postorbital process, the medial ridge is located anterior to mid-length, close to the anterior margin. The region in front of the medial ridge is thus very narrow, and the adductor region behind the medial ridge is wide and often continues onto the posteroventral process. On the suborbital process, the ridge is located ventral to mid-height, forming a wider orbital face. This condition is observed in examined members of Lacertidae, Scincidae and Teioidea (Fig. 1). Ontogenetic data show early (SMF 44976) and late (SMF 49566) juvenile Podarcis muralis and juvenile Lacerta agilis (SMF 49555) have the identical state as adults. This condition is also present in examined members of “Agamidae,” Iguaninae, Corytophaninae, and Tropidurinae as well as some polychrotines (Anolis ricordi, A. garmani, and Polychrus gutturosus) and anguimorphs, including Shinisaurus crocodilurus (Fig. 1D) and its fossil stem representative Merkurosaurus ornatus (Klembara, 2008), Lanthanotus borneensis and Celestus carraui (Fig. 1E). The jugal of Gobiderma pulchrum (extinct Late Cretaceous lizard; Borsuk-Białynicka, 1984) illustrated by Conrad et al. (2011b, Fig. 24) also appears to show type 1. The morphological constellation designated as type 1 is therefore widespread in lizards (Fig. 5). Type 1 is also found in Sphenodon punctatus. Ancestral character state reconstruction, regardless of broad-scale tree topology, supports this as the ancestral type for Squamata.
Type 2. The medial ridge on the suborbital process is ventrally located, as in type 1, but on the postorbital process it is located posterior to mid-length (it is posteriorly shifted). This condition is found in Restes rugosus (Fig. 2A), Exostinus serratus (Bhullar, 2010), and Xenosaurus newmanorum (Bhullar, 2011; Fig. 2B). The same condition is also observed in other anguimorphs such as Mesaspis (Fig. 2C) and Anniella pulchra. In addition to these anguimorphs, it is also present in Gerrhosaurus and Smaug (Fig. 2D,E), where ancestral state reconstruction shows that it must have arisen independently. Juveniles of Mesaspis monticola (DE 71, 72) have the same morphology as adults. It is additionally found in Eurheloderma sp. and Palaeosaniwa canadensis; both the former (Gilmore, 1928; Augé, 2005; Conrad, 2008), from the middle Eocene of Europe, and the latter (Balsai, 2001), from the Upper Cretaceous of the North America, are regarded as stem relatives of Heloderma. [Other opinions on Palaeosaniwa canadensis (Gilmore, 1928; Estes, 1964, 1983) were not based on the nearly complete MOR specimen, only fragments.]
Type 3. On the suborbital process, the medial ridge runs close to the dorsal margin, forming a large articulation area with the maxilla below it. The contact with the maxilla is long, reaching almost the level of posterior end of the suborbital process. This condition is observed in Chamaeleonidae (Fig. 3). Character optimization in Mesquite supports this as an autapomorphy of Chamaeleonidae, since the genus Brookesia is widely regarded as the extant sister clade to the remainder of Chamaeleonidae (Rieppel, 1987; Townsend and Larson, 2002; Townsend et al., 2011; Tolley et al., 2013). This state of character is also observed in fossil Lower Miocene taxon Chamaeleo andrusovi (see Čerňanský, 2010: fig. 4). Additionally, it has been found in chamaeleon-like lizard, Anolis barbatus.
On the postorbital process, the medial ridge is close to the anterior margin near the base, but departs sharply from the anterior margin dorsally. This is an artifact, however, of the unusual articulation with the postorbitofrontal, which is broad and extensive. Dorsally, the apparent medial ridge of the jugal actually just marks the posterior articulation with the postorbitofrontal. The orbital ridge of the jugal continues onto the ventrally extensive postorbitofrontal and is everywhere located near the anterior margin of the orbit.
B. The medial ridge is centrally located along the length of the jugal (Fig. 4).
Type 4. In contrast to types above, the course of the medial ridge here is close to the jugal's central axis on both suborbital and postorbital processes. This condition is present in Heloderma and some members of Anguidae (Anguinae and part of Gerrhonotinae—e.g., Barisia and Elgaria). Examined juveniles of Pseudopus apodus (DE 11), Ophisaurus and Anguis show the identical morphology as adult forms.
According to molecular phylogenies (Townsend et al., 2004; Hedges and Vidal, 2009; Vidal and Hedges, 2009; Wiens et al., 2012; Pyron et al., 2013), Xenosaurus, Heloderma, and Anguidae form a clade, Neoanguimorpha, to the exclusion of other anguimorphs. This result has not been achieved in any formal morphological analysis of anguimorph relationships (Estes et al., 1988; Lee and Caldwell, 2000; Evans et al., 2005; Conrad, 2008; Gauthier et al., 2012).
The medial ridge of the jugal provides a possible osteological synapomorphy of Neoanguimorpha (Fig. 5). To be sure, the course of this ridge is particularly variable in extant taxa referred to that clade. Extant anguids show types 1, 2, and 4; Xenosaurus shows types 1, 2, and 4 as well; and Heloderma shows type 4. Nevertheless, the phylogenetic relationships among Anguidae and successive fossil outgroups to Xenosaurus (Restes, Exostinus serratus) and Heloderma (Palaeosaniwa, Eurheloderma) support type 2 as the ancestral state of a clade including only those taxa, i.e., Neoanguimorpha. The character state change at the base of Neoanguimorpha is thus a posterior shift of the medial ridge on postorbital process. Subsequent modification, independently in Xenosaurus and Anguidae, involve reversal of this posterior shift on the postorbital process and/or a slight dorsal shift of the ridge on the suborbital process. Once the phylogenetic position of Gobiderma pulchrum has been resolved (cf., Gao and Norell, 1998; Conrad et al., 2011b; Gauthier et al., 2012), this species could play an important role in understanding the evolution of the medial ridge in Anguimorpha.
Similar changes are observed in Gerrhosaurus and Smaug (type 2). Thus, the medial ridge in Cordyliformes converges on that of some members of Anguimorpha.
Relationships of the Medial Ridge to Bony Orbital Structures
The orbit forms an opening in the skull that frames the eye and associated structures (muscles, optic nerve), and the jugal medial ridge supports the eye ventrally and posteriorly. It is therefore not surprising that the position of the eye is correlated with the course of the medial ridge. We are additionally concerned here with three aspects of the orbit: (1) The occurrence and position of bony structures (supraocular osteoderms, palpebral, supraorbital shelves of the frontal), which bound the eye dorsally; (2) the relation of the posterior process of the maxilla to the suborbital process of the jugal, which bound the eye ventrally; and (3) the angle of the jugal.
In type 1, the eye is located relatively ventrally. The suborbital process is therefore deeply hollowed out by the eye, and the medial ridge—the medial edge of the bone—depressed. The position of the eye influences, and is indicated by, the orientation of the supraorbital structures. Where supraocular osteoderms are present, as in Scincidae, Lacertidae, Shinisaurus, and Xenosaurus grandis, they do not bulge upwards. (This cannot be clearly ascertained in Lanthanotus, where the palpebral is minute and supraocular osteoderms poorly developed and medially located, but it is clear in whole specimens that the eye does not bulge dorsally.) Thus, the lateral exposure of the orbit—comprising that portion beneath the canthus—is depressed in lateral aspect. It is notable that type 1 is associated with two distinct configurations of the maxillo-jugal contact. In the plesiomorphic squamate condition (still seen in Sphenodon), the maxilla is posteriorly extensive, nearly reaching the posterior margin of the orbit (e.g., Lang, 1991; Conrad, 2004). The posterior process and the jugal strongly overlap in this region, and the orientation of the ectopterygoid is more lateral than anterior (see Smith, 2009; Gauthier et al., 2012). Bony supraorbital structures are largely absent. The same configuration is seen in many iguanians. In the second configuration, the maxilla extends less far posteriorly, and the ectopterygoid is oriented obliquely; supraorbital structures, especially palpebral and supraocular osteoderms, are present (e.g., Estes et al., 1988; Conrad, 2004; Bever et al., 2005). This configuration is seen in Scincoidea, Lacertiformes and taxa referred to Palaeoanguimorpha.
The configuration of the medial ridge that we have designated type 2 is noteworthy, given its potential phylogenetic significance, but also less well explained than the other types. In type 2, it appears that the eye is located relative posteriorly with respect to the postorbital process of the jugal. To the extent that type 2 and type 4 are similar, they both show a posterior shift of the ridge on the postorbital process. This may be related to a tightening of the angle (becoming less obtuse) between the suborbital and postorbital processes. Tiliqua rugosa appears to contradict this explanation in showing type 1 and a right-angled jugal, when the bone is taken in isolation (Fig. 1B); however, in the articulated skull, the postorbital process of the jugal is distinctly posteriorly angled because the suborbital process does not sit horizontally, possibly in consequence of its greatly reduced length. Many taxa referred to Neoanguimorpha have tight jugals, and even Xenosaurus newmanorum shows a steeper process than in other species of Xenosaurus (Fig. 6). However, it must be noted that the jugal does not form a right angle in Xenosaurus, and in Exostinus serratus the angle is even more open. A clear explanation is elusive. Given the phylogenetic hypothesis assumed here, type 2 phylogenetically precedes type 4.
In type 3, the eye is large and located more dorsally still. The suborbital process of the jugal has a horizontal orbital margin, as the eye is located chiefly above it. This reflects the large eyes associated with the highly developed sense of vision in this group and binocular vision reflecting the arboreal and prey-catching lifestyle (see e.g., Estes et al., 1988; Gioanni et al., 1993; Ott et al., 1998; King and Zhou, 2000). When supraorbital structures (namely, supraorbital flanges of the frontal) are present, these bulge strongly upwards. Thus, the lateral exposure of the orbit is rounded in lateral aspect. The convergent acquisition of a type 3 medial ridge in Chamaeleonidae and Anolis (“Chamaeleolis”) barbatus provides support for this hypothesis.
In type 4, the eye appears to be shifted from its primitively ventral position. The eye frequently appears to be located more dorsally, causing a weak or moderate dorsal bulge of the canthus by comparison with type 1 taxa, although not as dorsally as in type 3 taxa. The lateral exposure of the orbit has a moderately arched dorsal margin. Supraocular osteoderms are present, and the maxilla extends far posteriorly. Where it can be evaluated, a palpebral is also frequently present. [Notably, however, a palpebral is lacking in Heloderma, the only anguimorph known to lack it (Maisano et al., 2002; Gauthier et al., 2012). Whether a palpebral was present in Palaeosaniwa canadensis is presently unknown.] The orbit is elliptical in lateral aspect, but more rounded than in lacertids. The extent to which bulging occurs may depend on lifestyle and consequent head shape. In Pseudopus apodus, the head is relatively tall, and there is little or no dorsal bulging of the eye; in Xenosaurus platyceps, the head is flattened due to the rupicolous lifestyle, but the eye itself cannot be depressed. The relative influence of eye size is presently unclear; it is worth noting, however, that ontogenetic differences in jugal type, as might be expected due to negative allometry of eye size in ontogeny, were not observed.
Xenosaurus offers a unique opportunity to study this phenomenon in more detail, because the clade shows a variety of jugal configurations. In particular, X. grandis shows a depressed lateral aspect of the orbit, X. newmanorum a more elliptical shape, and in X. platyceps the lateral aspect of the orbit is distinctly rounded (dorsally bulging). How these observations relate to head form, eye size, and eye position may help clarify the proximate morphological causes of the observed configurations. Lifestyle is likely to be a critically important factor in this clade. Although all species are rupicolous (Ballinger et al., 1995; Lemos-Espinal et al., 2004; Lemos-Espinal et al., 2012) and show a flattened morphology, morphological differences could possibly be related to the size of crevices typically inhabited by the species. Because Exostinus serratus, also presents a type 2 jugal, it is reasonable to expect that the morphology of other orbital structures in that species was more similar to X. newmanorum than to any other.
The relation between organismal structure and function is generally assumed to be determined by the interaction of physical laws and evolutionary and developmental processes (Herrel et al., 2001). Adaptations consist of a number of components harmoniously integrated in a suitable, functional relationship (Frazzetta, 1975). In this case we have examined the relationship of the eye to the bony structures surrounding it: supraocular osteoderms, palpebral, maxilla, jugal, and ectopterygoid. However, the form of these bony structures is better seen as a developmental necessity. They are ineluctably shaped by the size and position of the eye, an early developing outgrowth of the central nervous system that precedes them in ontogeny and around which they condense.
The authors are greatly indebted to Dr. B.A.S. Bhullar (Harvard University) for the access to CT data of Restes rugosus. For critically reading the manuscript and the text corrections they thank two anonymous reviewers.