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The Atlasaxis Complex in Chamaeleonids (Squamata

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The Atlasaxis Complex in Chamaeleonids (Squamata THE ANATOMICAL RECORD 297:369–396 (2014) The Atlas-Axis Complex in Chamaeleonids (Squamata: Chamaeleonidae), With Description of a New Anatomical Structure of the Skull ANDREJ CER NANSK Y, 1,2* RENAUD BOISTEL,3 VINCENT FERNANDEZ,4,5 4 6 7 PAUL TAFFOREAU, NICOLAS LE NOIR, AND ANTHONY HERREL 1Senckenberg Research Institute and Natural History Museum Frankfurt, Palaeoanthropology and Messel Research, Frankfurt am Main, Germany 2Geological Institute, Slovak Academy of Sciences, Banska Bystrica, Slovakia 3IPHEP, Universite de Poitiers, UMR CNRS 6046, Pineau, Poitiers, France 4European Synchrotron Radiation Facility, Grenoble, Cedex 9, France 5Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, Johannesburg, South Africa 6Laboratoire Navier UMR8205, Champs-sur-Marne, France 7Departement d’Ecologie et de Gestion de la Biodiversite, UMR 7179 C.N.R.S/M.N.H.N., Paris Cedex, France ABSTRACT The comparative vertebral morphology of different chamaeleonid gen- era has been generally neglected and some aspects such as the compara- tive anatomy of the neck region remain poorly known. The atlas and axis of all chamaeleonid genera (Brookesia, Rieppeleon, Archaius, Rhampho- leon, Nadzikambia, Bradypodion, Chamaeleo, Calumma, Furcifer, Kinyongia, and Trioceros) are studied here. Considerable morphological differences are revealed. Additionally, some taxa exhibit sexual dimor- phism in the atlas and axis. An extremely long, divided posterodorsal pro- cess is present in males of the Trioceros johnstoni 1 Trioceros jacksonii clade. The solid and well-developed morphology of the posterodorsal pro- cess in males of this taxon could reflect its competitive behavior—males fight with their horns and attempt to dislodge one another from branches during encounters. An additional area of insertion for the cervical muscu- lature may indicate an incremental cervical musculature mass and cross sectional area that can add extra support and stability to the head and assist during combat involving lateral pushing. This character is not pres- ent in females. Heterochronic processes have played a role in the evolu- tion of chamaeleonids, as evidenced in many characters of the atlas–axis complex. A new hypothesis of an anterior shifting of synapophyses of the axis is erected and a new derived anatomical structure of the parietal of Chamaeleo calyptratus is described (the processus parietalis inferior). Grant sponsors: Alexander von Humboldt Foundation (Ger- Palaeoanthropology and Messel Research, Senckenberganlage many) and Vega Grant Agency; Grant number: 2/0087/13; 25, 60325 Frankfurt am Main, Germany. E-mail: Grant sponsor: Operational Programme Research and Develop- [email protected] ment as part of the project: Centre of Excellence for Integrated Received 22 April 2013; Accepted 5 July 2013. Research of the Earth’s Geosphere (ITMS); Grant number: DOI 10.1002/ar.22859 26220120064; Grant sponsors: European Regional Development Published online 31 January 2014 in Wiley Online Library Fund and Region Ile-de-France. (wileyonlinelibrary.com). *Correspondence to: Andrej Cer nansk y, Senckenberg Research Institute and Natural History Museum Frankfurt, VC 2014 WILEY PERIODICALS, INC. 370 CER NANSK Y ET AL. The presence of the processus parietalis inferior is associated with the evolution of the dorsally elevated parietal crest. Anat Rec, 297:369–396, 2014. VC 2014 Wiley Periodicals, Inc. Key words: Reptilia; comparative and functional anatomy; heterochrony; vertebrae; osteology specimens. In total we examined 21 chamaeleonid spe- INTRODUCTION cies, representing all described genera (Table 1)—Broo- Modern squamates represent a highly successful kesia (four species), Rieppeleon (one species), Archaius group of reptiles occupying a large range of habitats and (one species), Rhampholeon (two species), Nadzikambia showing a diversity of lifestyles. Some features of their (one species), Bradypodion (one species), Chamaeleo anatomy, especially their head and limbs, have been rel- (three species 1 data from others), Calumma (two spe- atively well-studied. In the past, numerous studies have cies), Furcifer (two species), Kinyongia (one species), and been published on the osteology of lizards, and many of Trioceros (three species). Additionally, several morpho- these studies provide data on vertebral morphology, logical characters from the following chamaeleonid speci- including that of chamaeleonids (e.g. Siebenrock, 1893; mens are examined (but not described in detail): Werner, 1902; Case, 1909; Methuen and Hewitt, 1914; Chamaeleo chamaeleon (ZFMK 21608), Chamaeleo dile- Hoffstetter and Gasc, 1969; Estes et al., 1988; Necˇas, pis (SMF 84618; ZFMK 5238), and T. hoehnelii (CMNH 1999; Bergmann et al., 2003; Al Hassawi, 2007). How- 144863). Hydrosaurus amboinensis (SMF 70930) and ever, the comparative vertebral morphology of different Shinisaurus crocodilurus (UF 71623) were also used to chamaeleonid genera has not been explored and details evaluate the synaphophyses. of the comparative anatomy of the neck region remain The specimens of Calumma globifer, Furcifer pardalis, poorly known, resulting in significant gaps in our knowl- and Chamaeleo calyptratus were photographed using a edge. Chamaeleons possess five cervical vertebrae, of which the first two are the atlas and axis (Hoffstetter and Gasc, 1969; Estes et al., 1988; Necˇas, 1999). This vertebral series is analyzed here for the species of the genera Brookesia, Rieppeleon, Archaius, Rhampholeon, Nadzikambia, Bradypodion, Chamaeleo, Calumma, Fur- cifer, Kinyongia, and Trioceros (for a phylogenetic tree depicting the species studied here, see Fig. 1). The atlas and axis interface with the basicranium (occipital con- dyle) allows the craniocervical movements (see e.g., Romer, 1956; Hoffstetter and Gasc, 1969). This skeletal bridge accommodates the origin and insertion of the anterior cervical musculature and provides insertion sites for tendons of the cervical muscles that help to sta- bilize the cranial region. It is reasonable to expect varia- tion in this complex among chamaeleonid taxa because of differences in cranial anatomy (see e.g., Rieppel, 1981; Rieppel and Crumly, 1997; Measey et al., 2009; Cer nansk y, 2010, 2011). The aims of this study are: (1) to describe in detail the morphology of the atlas and axis in various chamaeleo- nid taxa; (2) to compare their individual morphologies and study the role of heterochrony in the observed mor- phology; (3) to study male and female differences in selected taxa, reflecting their different behavior; and (4) to study the posterior region of the skull. MATERIAL AND METHODS Specimens Examined Skeletal material was obtained from museum collec- tions and from several captive bred specimens. Since problems with bone resorption exist (see e.g. Mader, Fig. 1. A phylogenetic metatree of chamaeleonid taxa studied here 2006; Hoby et al., 2010), a few structures are not well- (after Townsend and Larson, 2002; Rocha et al., 2005; Tilbury and preserved in some specimens. However, this problem has Tolley, 2009; Townsend et al., 2011; Crottini et al., 2012 and Glaw been easily resolved by supplementing them with other et al., 2012; Tolley et al., 2013). THE ATLANTO-AXIAL MORPHOLOGY OF CHAMAELEONIDS 371 TABLE 1. The list of specimens examined Chamaeleonid taxa 1 outgroup taxa No. specimens Collection numbers General information Uromastyx geyri 1 UF 44229 Adult Leiolepis belliana 2 SMF 57471; UF 62047 Adults Brookesia minima 1 MNHN1986.0876 Adult male Brookesia tristis 1 collection of M. Vences Adult Brookesia perarmata 1 MNHN 1993.0165 Adult female Brookesia thieli 1 A.H.& R.B. pers. coll. Adult female Rieppeleon brevicaudatus 1 A.H. & R.B. pers. coll. Adult female Archaius tigris 1 MNHN 1989.2872 Adult female Rhampoleon spectrum 4 RMCA R-73016.0093; MNHN Adults, male and female 1996.8001; 2 spec. A.C. pers. coll. Rhampoleon boulengeri 1 RMCA R-26570 Adult male Bradypodion occidentale 2 MNHN 1998.379 & 2000.2530 Adults Nadzikambia mlanjensis 2 PEM 16294 & PEM 18445 Adult male and female Chamaeleo namaquensis 2 MNHN 282 & A.H. pers. coll. Subadult and adult females Chamaeleo africanus 1 UMMZ 014181 Adult Chamaeleo calyptratus 11 DE 65, DE 74, DE 75, DE 76, From early juvenils to adults, DE 77, SAS—01 AC, SAS 02 males and females AC, SAS 04 AC, SAS 05 AC, SAS 08 AC, SAS 09 AC Furcifer pardalis 5 DE 80 – 81, SAS 03 AC, SAS Adults; DE males, SAS males 06 AC, SAS 07 AC and females Furcifer oustaleti 4 SMF 73684; SMF 59447; SMF Adult males 73685 and A.H. pers. coll. Calumma globifer 3 DE 82–84 Adults Calumma nasuta 1 MNHN 6643F Adult Kinyongia xenorhina 1 RMCA R-85003.0014 Adult Trioceros jacksoni 4 SMF 90037; A.C. pers.coll. Adult males and female Trioceros johnstoni 1 RMCA R-14150 Adult male Trioceros cristatus 1 RMCA R-28176 Adult scanning electron microscope (SEM—FEI Inspect F50) based on Tolley et al. (2013) for intergeneric relation- and a Nikon D 90 camera. Other photographs were ships, and Townsend et al. (2011), Townsend and Larson taken with a Leica M125 binocular microscope with axi- (2002), Rocha et al. (2005), Tilbury and Tolley (2009), ally mounted DFC500 camera; software: LAS (Leica Crottini et al. (2012) and Glaw et al. (2012) for intrage- Application Suite) version 4.1.0 (build 1264). neric relationships. The taxa Uromastyx geyri and Leio- Institutional Abbreviations used: CMNH 5 Carne- lepis belliana were used for the outgroup comparison. gie Museum of Natural History, Pittsburgh, USA; DE 5 Faculty of Natural Sciences, Comenius
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