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The Relationship Between Cephalic Scales and Bones in Lizards: a Preliminary Microtomographic Survey on Three Lacertid Species

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The Relationship Between Cephalic Scales and Bones in Lizards: a Preliminary Microtomographic Survey on Three Lacertid Species THE ANATOMICAL RECORD 293:183–194 (2010) The Relationship Between Cephalic Scales and Bones in Lizards: A Preliminary Microtomographic Survey on Three Lacertid Species DAVID COSTANTINI,1 MARIA LAPRESA ALONSO,2 MEHRAN MOAZEN,3,4 2 AND EMILIANO BRUNER 1Division of Ecology and Evolutionary Biology, Faculty of Biomedical and Life Sciences, University of Glasgow, Graham Kerr Building, Glasgow, United Kingdom 2Centro Nacional de Investigacio´n sobre la Evolucio´n Humana, Burgos, Spain 3Department of Engineering, University of Hull, Hull, United Kingdom 4School of Mechanical Engineering, University of Leeds, Leeds, United Kingdom ABSTRACT In the last two decades, there has been a great deal of interest in the morphology and anatomy of the lizard skull in an ecological and evolu- tionary perspective. However, the relationship between variations in many key anatomical features remains largely unknown. Using microto- mography and geometric morphometrics, we examined the relationship between bones and scales associated with the parietal foramen in the three lizards species most common in the Italian peninsula: Podarcis muralis, P. sicula, and Lacerta bilineata. The imprints of the scales are clearly recognizable on the outer bone surface, and this may suggest a structural interaction between these elements. The temporal osteoderms are visible in the larger males and in the larger females of L. bilineata, but they are absent in the smaller specimens of L. bilineata and in all Podarcis specimens. Two parallel rows of pterygoid teeth are present in all the specimens of L. bilineata and are absent in the smaller male of L. bilineata and in both Podarcis species. Cheek osteoderms occurred only in the largest specimens of our sample (i.e., large L. bilineata), being possibly related to hyperostotic processes and densitometric thresholds more than to phylogeny. Minor differences may be also associated with the form of the parietal foramen. In absolute terms the parietal foramen tends to be largest in L. bilineata but in relation to skull length the fora- men tends to be larger in P. muralis. In this latter species the foramen is also more elongated. In all three species the fronto-parietal suture occu- pies a similar location relatively to the scale spatial organization. A shared allometric pattern shows that the main vault enlargement can be localised at the areas anterior to the fronto-parietal suture, providing fur- ther information on the possible morphogenetic dynamics associated with the interaction between scales and bones around this structure. Anat Rec, 293:183–194, 2010. VC 2009 Wiley-Liss, Inc. Key words: lacertids; cranial anatomy; tomography; fronto-parietal suture; Podarcis; Lacerta *Correspondence to: Emiliano Bruner, Centro Nacional Received 16 June 2009; Accepted 27 August 2009 de Investigacio´n sobre la Evolucio´n Humana, Paseo de Ata- DOI 10.1002/ar.21048 puerca s/n, 09002 Burgos, Spain. E-mail: emiliano.bruner@ Published online 28 November 2009 in Wiley InterScience cenieh.es (www.interscience.wiley.com). VC 2009 WILEY-LISS, INC. 184 COSTANTINI ET AL. INTRODUCTION between species, providing helpful information on the structural organization of the skull (Hallgrimsson et al., The lizard family Lacertidae comprises about 280 spe- 2007). Lacertids are one of the most diverse groups of liz- cies distributed throughout Eurasia and Africa (Arnold ards in terms of dietary specialization, and although they et al., 2007). The fossil history of the family extends have been well described in the literature (e.g., Arnold, back at least to the Lower Eocene, about 45–50 My ago 1989; Barahona and Barbadillo, 1998; Herrel et al., 2004, (Bo¨hme and Weitschat, 1998, 2002; Borsuk-Bialynicka 2008; Evans, 2008), the degree to which the mechanics of et al., 1999; Evans, 2003; Hipsley et al., 2009). Despite their skulls differs among species remains unexamined. the large amount of investigation, the phylogenetic rela- In this study, we carried out an exploratory computed tionships within this family are still not completely microtomography (lCT) survey together with morpho- understood (Arnold, 1973; Oliverio et al., 1998, 2000; metric analyses to supply information on cranial anat- Harris et al., 2005; Arnold et al., 2007). omy and morphology and on the relationships between In the last two decades, there has been a great deal of scales and bones in the three lacertid species: the com- interest in interspecific and intraspecific variation in the mon wall lizard Podarcis muralis (Laurenti, 1768), the morphology and anatomy of lizard skull (bones, scales, Italian wall lizard Podarcis sicula (Rafinesque-Schmaltz, osteoderms) to obtain new insights into lizard evolution 1810) and the western green lizard Lacerta bilineata (e.g., Arnold, 1989; Barahona and Barbadillo, 1998; (Daudin, 1802). All the three species represent the most Metzger, 2002; Arnold et al., 2007). An anatomical report common lizard species in the Italian peninsula, although on the ossification of lacertid skull shows that the bones they can be found elsewhere in Europe (Arnold and Bur- of the snout region (premaxilla, maxilla and nasal bones) ton, 1978; Corti and Lo Cascio, 1999; Sindaco et al., ossify before those of the skull roof, and the posterior 2006; see for a general description of anatomy Barahona region of the frontal areas ossifies before the anterior and Barbadillo, 1998; Arnold et al., 2007). They belong region of the parietals (Barahona and Barbadillo, 1998). to the tribe Lacertini (around 108 species). The molecu- An equivalent of similar antero-posterior growth gradi- lar differences suggest that this tribe diversified around ent, associated with a differential allometric rate, has 12–16 My ago, producing three main evolutionary units been described in several lacertids, as well as in other (Arnold et al., 2007): the Lacerta-Timon clade of large- lizard taxa, in both the skull (Monteiro and Abe, 1997) bodied lizards probably dispersed earliest, followed by and the cephalic scales (Bruner et al., 2005; Bruner and Algyroides and then Podarcis. This study is aimed at Costantini, 2007). The fronto-parietal suture, which is providing information on specific anatomical cranial positioned under the fronto-parietal scales, has been traits in these Mediterranean lizards, and on the varia- hypothesized to be a relevant pace-maker of the head tion of some neurocranial structures related to the growth and development (Bruner and Costantini, 2007). cranial morphogenetic dynamics. The degree of interdigitation at the fronto-parietal suture restricts dorsoventral bone movements, modulat- ing the cranial kinesis (Barahona and Barbadillo, 1998; MATERIALS AND METHODS l Metzger, 2002). In addition to anatomical constraints, Sampling and CT Analysis diet and mating both have a role in shaping the head The sample includes specimens of P. muralis, P. sicula, morphology (including both bones and cephalic scales), and L. bilineata collected as prey remains from nest- mostly through the stress generated by muscles (jaw boxes of Eurasian kestrels Falco tinnunculus (Costantini adductors and nuchal attachments) involved in feeding, et al., 2005, 2007). Prey remains were used only when coupling, or fighting (Moss and Young, 1960; Buckland- the preservation was sufficient enough to investigate Wright, 1978; Bruner et al., 2005; Huyghe et al., 2009). head morphology and recognize the species. All the indi- The muscular system may exert structural pressures viduals were recovered around Rome, between 1999 and and tensions on the surrounding anatomical elements; 2005. Of each species, we included in this study three however, bones may represent a morphogenetic pace- males and three females chosen from a larger sample maker in many cephalic regions by means of modulator (Bruner et al., 2005; Bruner and Costantini, 2007) in structures, such as the fronto-parietal suture. order to have a head size gradient (i.e., from small to It is widely accepted that morphological differences large) for each sex and for each species, respectively. between species reflect differences in diet, ecology and The specimens were scanned using a high-resolution patterns of bone growth (Moreno and Carrascal, 1993; X-ray microtomography (lCT-80, Scanco Medical, Swit- Niehoff et al., 2004; Herrel et al., 2008; but see Schwenk, zerland), at 45 kV X-ray tube voltage, 88 lA, 0.35 degree 2000, 2002). The way such morphological differences have rotation step and 800 ns exposure time per individual evolved may provide useful information on morphogenetic shadow projection. The voxel size was 36 Â 36 Â 36 lm, patterns and selective pressures acting on them. Morpho- with an average exposure time of 120 min per scan. CT genesis is a polyphasic and multifactorial process in which data analysis, automatic and semiautomatic segmenta- a genetic program is decoded through the interaction with tion, surface rendering, and traditional metrics, were environmental factors and expressed within a given bio- performed using Mimics 11.11 (Materialise, Belgium). mechanical context (Cheverud, 1996; Klingenberg, 2002). In this framework, functional morphometrics largely deals Anatomy and Morphometrics with the biomechanical environment, trying to identify, describe, and understand the structural relationships The microtomographic sections and the computed sur- between the elements of the anatomical system (Moss and face reconstructions were used to investigate anatomical Young, 1960). Under this scenario, applications of geomet- differences between the
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