Received: 6 July 2017 | Accepted: 4 November 2017 DOI: 10.1111/zsc.12266 ORIGINAL ARTICLE Evolutionary history of spiny- tailed lizards (Agamidae: Uromastyx) from the Saharo- Arabian region Karin Tamar1 | Margarita Metallinou1† | Thomas Wilms2 | Andreas Schmitz3 | Pierre-André Crochet4 | Philippe Geniez5 | Salvador Carranza1 1Institute of Evolutionary Biology (CSIC- Universitat Pompeu Fabra), Barcelona, The subfamily Uromastycinae within the Agamidae is comprised of 18 species: three Spain within the genus Saara and 15 within Uromastyx. Uromastyx is distributed in the 2Allwetterzoo Münster, Münster, Germany desert areas of North Africa and across the Arabian Peninsula towards Iran. The 3Department of Herpetology & systematics of this genus has been previously revised, although incomplete taxo- Ichthyology, Natural History Museum of nomic sampling or weakly supported topologies resulted in inconclusive relation- Geneva (MHNG), Geneva, Switzerland ships. Biogeographic assessments of Uromastycinae mostly agree on the direction of 4CNRS-UMR 5175, Centre d’Écologie Fonctionnelle et Évolutive (CEFE), dispersal from Asia to Africa, although the timeframe of the cladogenesis events has Montpellier, France never been fully explored. In this study, we analysed 129 Uromastyx specimens from 5 EPHE, CNRS, UM, SupAgro, IRD, across the entire distribution range of the genus. We included all but one of the rec- INRA, UMR 5175 Centre d’Écologie Fonctionnelle et Évolutive (CEFE), PSL ognized taxa of the genus and sequenced them for three mitochondrial and three Research University, Montpellier, France nuclear markers. This enabled us to obtain a comprehensive multilocus time- calibrated phylogeny of the genus, using the concatenated data and species trees. We Correspondence Karin Tamar, Institute of Evolutionary also applied coalescent- based species delimitation methods, phylogenetic network Biology (CSIC-Universitat Pompeu Fabra), analyses and model- testing approaches to biogeographic inferences. Our results re- Barcelona, Spain. vealed Uromastyx as a monophyletic genus comprised of five groups and 14 inde- Email: [email protected] pendently evolving lineages, corresponding to the 14 currently recognized species Funding information Uromastyx Secretaria d’Universitats i Recerca del sampled. The onset of diversification is estimated to have occurred in Departament d’Economia i Coneixement de south- west Asia during the Middle Miocene with a later radiation in North Africa. la Generalitat de Catalunya, Grant/Award During its Saharo-Arabian colonization, Uromastyx underwent multiple vicariance Number: 2014-SGR-1532; Ministerio de Economía y Competitividad, Spain and dispersal events, hypothesized to be derived from tectonic movements and habi- (cofunded by FEDER), Grant/Award tat fragmentation due to the active continental separation of Arabia from Africa and Number: CGL2015-70390-P the expansion and contraction of arid areas in the region. KEYWORDS agamids, Arabia, biogeography, multilocus phylogeny, reptiles, systematics 1 | INTRODUCTION two genera, Saara Gray, 1845 (three species; Irano- Turanian region; Iraq, Iran, Afghanistan, Pakistan, and India) and The Uromastycinae Theobald, 1868 is a subfamily within Uromastyx Merrem, 1820 (15 species; Saharo- Arabian re- Agamidae, distributed in the desert belt of the Old World, gion; from the Atlantic coast of north- west Africa to Iran) and is phylogenetically the sister subfamily to the rest of the (Sindaco & Jeremčenko, 2008; Uetz, Freed, & Hzrošek, Agamid taxa (Macey et al., 2000; Pyron, Burbrink, & Wiens, 2017; Wilms, 2005; Wilms, Böhme, Wagner, Lutzmann, 2013; Townsend et al., 2011). This subfamily is comprised of & Schmitz, 2009). Uromastycinae members are commonly called spiny- tailed lizards due to the shape of their tail cov- †Deceased July 2015. ered by spiny scales arranged in distinct whorls. The two Zoologica Scripta. 2018;47:159–173. wileyonlinelibrary.com/journal/zsc © 2017 Royal Swedish Academy of Sciences | 159 160 | TAMAR ET AL. genera, Saara and Uromastyx, are differentiated by the pres- partially established in the previously mentioned studies, ence or absence of intercalaries between the tail whorls, re- although incomplete taxonomic sampling or several weakly spectively (Wilms, 2005; Wilms et al., 2009). Spiny- tailed supported topologies resulted in inconclusive relationships. lizards are ground dwelling or saxicolous, predominantly The biogeographic history of Uromastycinae in general herbivorous, characterized by their medium to large size, and that of Uromastyx in particular was evaluated in several their spiny whorled tail and a distinctive diagnostic denti- studies, suggesting a general dispersal from east to west (e.g., tion (Moody, 1980; Wilms, 2005). These lizards have a stout Amer & Kumazawa, 2005a; Moody, 1980; Wilms et al., depressed habitus with stubby limbs, and their body is usu- 2009). From central or southern Asia, Uromastycinae dis- ally covered with small homogeneous scales, although some persed westwards into south-western Asia, Arabia and North members have additional scattered tubercular scales (Wilms, Africa, most likely during the Eocene–Oligocene onwards, 2005; Wilms & Böhme, 2001). Uromastycinae members with the progression of suitable arid habitats in these regions. have long been a part of the reptile pet trade, with reports Although the direction of this divergence from Asia to Africa dating to the 19th century (e.g., von Fischer, 1885). These liz- is agreed upon by most studies, the timeframe of these cladoge- ards are registered in appendix II of CITES (www.cites.org) netic events has never been fully explored. Divergence-time due to their extensive collection for food, medicine, and local estimates targeting the Uromastycinae members have only and international pet trade (Ching & Chng, 2016; Knapp, been assessed by two prior studies (i.e., Amer & Kumazawa, 2004; Mahmood, Shah, Rais, & Nadeem, 2011; Pechmann, 2005a; Joger, 1986), based on ND2-tRNAs amino acid and Scott, Semlisch, Caldwell, & Vitt, 2005; Robinson, Griffiths, nucleotide distances and on immunological distance data, John, & Roberts, 2015). In the IUCN Red List of Threatened respectively. These two studies suggested that the species Species (http://www.iucnredlist.org), of the nine listed spe- now classified within Saara and Uromastyx started diverg- cies of the subfamily, three are listed as Near Threatened and ing during the Oligocene, approximately 25–30 million years two as Vulnerable. ago (Mya). Amer and Kumazawa (2005a) hypothesized that Uromastyx, the largest genus within the Uromastycinae, an initial stage of radiation probably occurred in the eastern inhabits desert areas and ranges across North Africa, in- Middle East, prior to the connection between Africa and cluding the Sahel and the Horn of Africa, eastwards to Eurasia ca. 18 Mya (i.e., the Gomphotherium land bridge; Iran through the Arabian Peninsula and northwards to cen- Rögl, 1998), and that the ancestor of Uromastyx most likely tral Syria and Iraq (Figure 1; Wilms, 2005; Sindaco & derived from this region. According to their estimates, Jeremčenko, 2008; Wilms & Schmitz, 2007; Uetz et al., the Uromastyx radiation during the Middle Miocene ca. 2017). Uromastyx mainly occurs in deserts and semi- desert 11–15 Mya may have occurred due to an aridification pro- habitats of compacted ground (they do not occur on sand cess in the area, which facilitated migration and cladogenesis dunes), covered with rocks, scattered stones, gravel and between and within Arabia and Africa. sparse vegetation (Arnold, 1980; Wilms, 2005). The tax- The Saharo- Arabian region, spanning across North Africa onomy of Uromastyx has changed through the years, with and Arabia, is a unique region for evolutionary and biogeo- four species and three subspecies described since 1980 (see graphic research. The region has a long and complex geo- Uetz et al., 2017). Morphological revisions of Uromastyx logical history of suturing and rifting—it covers both the (e.g., Mateo, Geniez, Lopez- Jurado, & Bons, 1999; Wilms, active continental separation of Arabia from Africa at the 2001; Wilms & Böhme, 2000a, 2000b, 2001, 2007; Wilms & Red Sea and the collision zone of the African- Arabian plates Schmitz, 2007; Wilms et al., 2009) and molecular phyloge- with the Eurasian landmass at its northern edge (Bohannon netic studies (e.g., Amer & Kumazawa, 2005a, 2009; Harris, 1989; Girdler, 1991; Ghebreab, 1998; Popov et al., 2004; Vaconcelos, & Brito, 2007; Wilms & Schmitz, 2007; Wilms Bosworth, Huchon, & McClay, 2005). This tectonically ac- et al., 2009; Amin & Amer, 2011; Amer, Ahmed, Wilms, tive region has undergone drastic climatic changes with pro- Shobrak, & Kumazawa, 2012) have contributed greatly to found aridification processes followed by hyperarid areas our understanding of the intra- and interspecific relationships alternately expanding and contracting (Le Houérou, 1992, within the genus. Uromastyx taxa are currently divided into 1997). Periodic terrestrial connectivity between Africa and the following five groups: U. acanthinura group (African; Arabia through the Red Sea, and between Afro- Arabia and five species), U. aegyptia (Arabian; one species), U. ocellata Asia (through the Gomphotherium land bridge), coupled group (Arabian; five species), U. princeps group (African; with climatic oscillations are hypothesized to have enabled two species) and U. thomasi (Arabian; one species). The multiple vicariance and dispersal events, and phases of fau- phylogenetic