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On the Phylogeny and Taxonomy of the Genus Uromastyx Merrem, 1820 (Reptilia: Squamata: Agamidae: Uromastycinae) – Resurrection of the Genus Saara Gray, 1845

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On the Phylogeny and Taxonomy of the Genus Uromastyx Merrem, 1820 (Reptilia: Squamata: Agamidae: Uromastycinae) – Resurrection of the Genus Saara Gray, 1845 Bonner zoologische Beiträge Band 56 (2007) Heft 1/2 Seiten 55–99 Bonn, März 2009 On the Phylogeny and Taxonomy of the Genus Uromastyx Merrem, 1820 (Reptilia: Squamata: Agamidae: Uromastycinae) – Resurrection of the Genus Saara Gray, 1845 Thomas M. WILMS1),4), WOLFGANG BÖHME2), Philipp WAGNER2), Nicolà LUTZMANN2) & Andreas SCHMITZ3) 1)Zoologischer Garten Frankfurt, Bernhard-Grzimek-Allee 1, D-60316 Frankfurt am Main, Germany; E-Mail: [email protected]; 2)Zoologisches Forschungsmuseum A. Koenig, Adenauerallee 160, D- 53113 Bonn, Germany; 3)Muséum d’Histoire naturelle, C. P. 6434, CH-1211 Genève 6, Switzerland; 4)Corresponding author Abstract. We assessed the taxonomic relationships within the genus Uromastyx Merrem, 1820 using morphologi- cal and genetic methods, resulting in the resurrection of the genus Saara Gray, 1845 for Saara hardwickii, S. as- mussi and S. loricata and in changes of the taxonomic rank of Uromastyx nigriventris, U. aegyptia leptieni and U. shobraki. A synopsis of all taxa considered to be valid is provided, including differential diagnosis, description and data on their respective distribution. A key for the species of Saara and Uromastyx is presented. Keywords. Reptilia; Sauria; Agamidae; Uromastycinae; Uromastyx; Saara; Saara hardwickii; Saara asmussi new comb.; Saara loricata new comb.; Uromastyx aegyptia leptieni new status; Uromastyx nigriventris new status; Uromastyx sho- braki new status; Phylogeny; Taxonomy; Morphology. 1. INTRODUCTION Within the Palearctic genus Uromastyx Merrem, 1820 a (KNAPP 2004, WILMS 2007a). But the consumption of total of 17 species are considered to be valid by WILMS spiny-tailed lizards in their countries of origin may be con- & SCHMITZ (2007) and WILMS & BÖHME (2007). Some of siderably higher due to the fact, that Uromastyx are heav- the species respective subspecies belonging to that genus ily hunted for food and for the production of souvenirs and have been described quite recently (e. g. Uromastyx dis- traditional medicine (WILMS 2007a). par maliensis Joger & Lambert, 1996; Uromastyx occi- dentalis Mateo et al., 1998; Uromastyx leptieni Wilms & The main aim of the present paper is to evaluate the phy- Böhme, 2000; Uromastyx alfredschmidti Wilms & Böhme, logenetic relationships within the taxa of the genus Uro- 2001; Uromastyx y. yemenensis Wilms & Schmitz, 2007, mastyx and to establish a hypothesis of the taxonomy of and Uromastyx y. shobraki Wilms & Schmitz, 2007) re- this group, based on a synthesis of morphological and ge- flecting a continuing scientific interest in the phylogeny netic characters. and taxonomy of these animals. Taxonomic History Uromastyx spp. are medium sized to large lizards inhab- iting the old world desert belt from North Africa to north The taxonomic history of the lizards currently assigned western India. All species are either ground dwellers or to the genus Uromastyx dates back to the second half of saxicolous, with some species climbing occasionally on the 18th century [description of Lacerta aegyptia trees. Uromastyx are predominantly herbivorous, feeding FORSSKÅL, 1775; for more detailed information on the his- on the scarce vegetation in their desert environment. Eco- tory of this taxon see WILMS & BÖHME 2000 a. For a dis- logically these animals are largely limited by the availabil- cussion on the spelling of PEHR FORSSKÅL’s family name ity of food and by the availability of appropriate thermal see FRIIS & THULIN (1984)]. refuges. The genus name Uromastyx was coined by MERREM in his Uromastyx spp. are currently listed on Appendix II of work ‘Versuch eines Systems der Amphibien – Tentamen CITES. Internationally more than 367 000 specimens have Systematis Amphibiorum’ (MERREM 1820). Of the seven been traded legally in the pet trade between 1977 and 2005 species included in this first synopsis of the genus only 56 Thomas M. WILMS et al.: On the Phylogeny and Taxonomy of the Genus Uromastyx Merrem, 1820 one is belonging to Uromastyx as it is currently defined tional Museum, Museum of Natural History Prague [Uromastyx spinipes (Daudin, 1802) = Uromastyx aegyp- (NMP6V); Naturmuseum und Forschungsinstitut Senck- tia (Forsskål, 1775)]. enberg, Frankfurt a. M. (SMF); Zoologisches Forschungsmuseum A. Koenig, Bonn (ZFMK); Zoologi- Between 1822 and 1885 a total of five new genera (Mas- sches Museum der Universität Hamburg (ZMH); Muse- tigura Fleming, 1822; Centrocercus Fitzinger, 1843; Saara um für Naturkunde, Humbold-Universität, Berlin (ZMB) Gray, 1845; Centrotrachelus Strauch, 1863; Aporoscelis and Zoologische Staatssammlung München (ZSM). For Boulenger, 1885) were erected for different members of a list of examined specimens see Appendix II. the genus Uromastyx of which only Aporoscelis and Cen- trotrachelus were considerably in use (e. g. ANDERSON For each specimen 25 external characters (16 meristic, 6 1894, 1896, 1901; BLANFORD 1874, 1881; VON BEDRIA- metric, 3 qualitative) have been routinely recorded: snout- GA 1879; MURRAY 1884; SCORTECCI 1933; NINNI 1933; vent length (SVL), length of tail (TL), head width between PARKER 1942; HAAS & WERNER 1969). Aporoscelis was the anterior margins of the ear openings (HW), head length used in the rank of a subgenus by JOGER (1987). The name from the tip of the snout to the anterior margin of the ear Centrocercus Fitzinger, 1843 is preoccupied by Centro- opening on the left side (HL), width of tail between the cercus Swainson, 1832 (Aves, Phasianidae) and is there- 4th and 5th whorl (TW), maximum tail width at the 5th fore not available. The main taxonomic problem within whorl (TWmax), number of tail whorls (W), number of Uromastyx was the proper delimitation of taxon bound- scales beneath the 4th toe on the left side (SD), number of aries on the specific and subspecific level, which led in gular scales (from mental to a line between the anterior the past to considerable confusion on the identity of di- margins of the ear openings (G)), number of scales around verse taxa (for more detailed information see WILMS & mid-body (MBS), number of scales between gular- and BÖHME 2000 a, 2000 b, 2001). inguinal fold (V; ventrals), number of scales around the 5th whorl (SW), number of preanofemoral pores (PP; left Beside studies based on external morphology (e. g. and right), number of enlarged scales at the anterior mar- MERTENS 1962; MOODY 1987; WILMS & BÖHME 2000 a, gin of the ear opening (LS; left and right), number of 2000 b; WILMS & BÖHME 2001; WILMS & SCHMITZ 2007) scales between suboculars and supralabials (SO; left and and immunology (JOGER 1987), some recent papers also right), number of scales from the mid of the lower end of adress this issue by employing molecular genetic meth- the ear opening to the mental scale (HS; left and right), ods (AMER & KUMAZAWA 2005; WILMS & SCHMITZ 2007; number of scales from the upper to the lower end of the HARRIS et al. 2007). Nevertheless some aspects of the tax- left ear opening (ES; approximately three scale rows be- onomy of these highly specialized desert lizards still re- fore the anterior margin of the ear opening), number of main unclear. scales from the upper end of the left ear opening to the first enlarged subocular scale (PES), presence or absence On the basis of external morphology and immunological of enlarged tubercular scales at the flanks (TF; absent = distances it is well established, that several species groups 0 / present = 1), enlarged tubercular scales at the dorsum within Uromastyx are recognizable, but the relationships (TD; absent = 0 / present = 1 / arranged in rows = 2), in- and species compositions of these groups are still under tercalary scales between the whorls present or absent (IS; debate (JOGER 1986; MOODY 1987; WILMS 2001; AMER absent = 0 / 1–2 unkeeled present = 1 / 2–6 keeled pres- & KUMAZAWA 2005; WILMS & SCHMITZ 2007). ent = 2). Measurements were taken to the nearest 0.5 mm using a calliper. 2. MATERIAL AND METHODS To obtain morphological outgroup data from the closest relatives of Uromastyx several vouchers of the genus Morphological sampling and analysis Leiolepis from the collection of the ZFMK were exam- ined. 621 specimens of the genus Uromastyx, including the type material of the relevant taxa have been examined. The Statistical analyses of morphological data specimens are deposited in the following collections (In- stitutional abbreviations in parenthesis): The Natural His- The Excel 2000 and SPSS (10.0) statistical packages were tory Museum, London (BMNH); Naturhistorisches Mu- used to run the analyses. Hierachical Cluster analysis and seum Wien (NMW); Museo Zoologico de „La Specola“, Principal Component Analysis (PCA) have been selected Firenze (MZUF); Muséum d’Histoire Naturelle, Genève to evaluate the morphological data and to explore the phe- (MHNG); Muséum National d’Histoire Naturelle, Paris netic relationships between the taxa examined. (MNHN); Museum für Tierkunde, Dresden (MTKD); Na- Bonner zoologische Beiträge 56 (2007) 57 Phylogenetic analysis of morphological data To get a better resolution within two identified clades of very closely related taxa (compare below), 12S rRNA da- Phylogenetic analysis was carried out on the basis of twen- ta for representatives of those clades were added and sep- ty-five external characters (16 meristic, 6 metric, 3 qual- arate trees were produced. Therefore, in these cases we itative). To assign a polarity to these characters (plesiomor- amplified a section of the mitochondrial 12S ribosomal phy vs. apomorphy), ingroup and outgroup comparisons RNA gene using the primers 12SA-L (light chain; 5’ - were applied (WATROUS & WHEELER 1981; MADDISON et AAA CTG GGA TTA GAT ACC CCA CTA T - 3’) and al. 1984). Species of the genus Leiolepis were used as out- 12SB-H (heavy chain; 5’ - GAG GGT GAC GGG CGG group, because this genus forms the morphologically and TGT GT - 3’) of KOCHER et al. (1989). Cycling procedure genetically proposed sister clade to Uromastyx (PETERS was again identical as described in SCHMITZ et al. (2005). 1971; BÖHME 1988; SCHMITZ et al. 2001; AMER & KU- MAZAWA 2005). Within the genus Leiolepis seven taxa are PCR products were purified using Qiaquick purification distinguished: L.
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