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Molecular Phylogeny and Historical Biogeography of the Anatolian Lizard Apathya (Squamata, Lacertidae)

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Molecular Phylogeny and Historical Biogeography of the Anatolian Lizard Apathya (Squamata, Lacertidae) Molecular Phylogenetics and Evolution 66 (2013) 992–1001 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny and historical biogeography of the Anatolian lizard Apathya (Squamata, Lacertidae) Paschalia Kapli a,b,1, Dimitra Botoni a,b,1, Çetin Ilgaz c,1, Yusuf Kumlutasß c, Aziz Avcı d, Nasrullah Rastegar-Pouyani e, Behzad Fathinia e, Petros Lymberakis a, Faraham Ahmadzadeh f,g, ⇑ Nikos Poulakakis a,b, a Molecular Systematics Lab, Natural History Museum of Crete, University of Crete, 71409 Iraklion, Crete, Greece b Biology Department, University of Crete, 71409 Iraklion, Crete, Greece c Dokuz Eylül University, Faculty of Science, Department of Biology, 35160 Buca/Izmir,_ Turkey d Adnan Menderes University, Faculty of Science and Arts, Department of Biology, 09010 Aydın, Turkey e Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran f Department of Biodiversity and Ecosystem Management, Environmental Sciences Research Institute, Shahid Beheshti University, Evin, Tehran, Iran g ZoologischesForschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany article info abstract Article history: Apathya is a lacertid genus occurring mainly in south-east Turkey and its adjacent regions (part of Iran Received 7 August 2012 and Iraq). So far two morphological species have been attributed to the genus; A. cappadocica (with five Revised 23 November 2012 subspecies, A. c. cappadocica, A. c. muhtari, A. c. schmidtlerorum, A. c. urmiana and A. c. wolteri) and A. yas- Accepted 5 December 2012 sujica. The first species occupies most of the genus’ distribution range, while A. yassujica is endemic of the Available online 20 December 2012 Zagros Mountains. Here, we explored Apathya’s taxonomy and investigated the evolutionary history of the species by employing phylogenetic and phylogeographic approaches and using both mitochondrial Keywords: (mtDNA) and nuclear markers. The phylogenetic relationships and the genetic distances retrieved, Anatolian Diagonal revealed that Apathya is a highly variable genus, which parallels its high morphological variation. Such Divergence times Mitochondrial DNA levels of morphological and genetic differentiation often exceed those between species of other Lacertini Molecular systematics genera that are already treated as full species, suggesting the necessity for a taxonomic revision of Apat- Nuclear DNA hya. The phylogeographical scenario emerging from the genetic data suggests that the present distribu- Phylogeography tion of the genus was determined by a combination of dispersal and vicariance events between Anatolia and Southwest Asia dating back to the Miocene and continuing up to the Pleistocene. Key geological events for the understanding of the phylogeography of the genus are the movement of the Arabian plate that led to the configuration of Middle East (orogenesis of the mountain ranges of Turkey and Iran) and the formation of Anatolian Diagonal. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction subgenera Podarcis and Gallotia to the generic level. In this revision, Lacerta was divided into two groups: Lacerta part I which is more The lizard family Lacertidae consists of about 280 species placed or less equivalent to Lacerta sensu stricto and Lacerta part II. The in 24–30 genera found throughout Eurasia and Africa (Arnold et al., former encompasses large bodied Lacerta species, usually 2007). Based on morphology most of the recognized genera appear occurring in areas of dense and shrubby vegetation, while the lat- to be included in monophyletic clades, with the exception of the ter consists of smaller bodied species, many of them saxicolous. paraphyletic central African Adolfus and Lacerta sensu lato of The systematics of Arnold’s (1973) Lacerta part II is far from Europe, SW and N Asia and northwest Africa. being resolved. Some species groups previously assigned to Lacerta The genus Lacerta, a morphologically extremely diverse are now grouped in different genera or subgenera (Arnold et al., genus, was initially revised by Arnold (1973) who separated four 2007; Mayer and Arribas, 2003) with unknown relationships tropical and southern African species from Lacerta and raised the among them. One of them is the medium size lacertid lizard of the genus Apathya, first described from Erciyes Mountain in Kayseri, Turkey (Ilgaz et al., 2010). ⇑ Corresponding author at: Molecular Systematics Lab, Natural History Museum of Crete and Biology Department, University of Crete, Iraklion, Crete, Greece. Nowadays, Apathya Mehely, 1907 includes 2 species [Apathya E-mail address: [email protected] (N. Poulakakis). cappadocica (Werner, 1902) and A. yassujica (Nilson et al., 2003)] 1 These author contributed equally to this work. and occurs (Fig. 1) in Central, East, and South Anatolia, Northern 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.12.002 P. Kapli et al. / Molecular Phylogenetics and Evolution 66 (2013) 992–1001 993 Anatolian Diagonal Acm1-4 Acm8 Acc2 Acc5 Acc4 Acm10 Acc6 Acc3 Asch1-2 Acc1 Acw7-8 Acw9-10 Acu1-2 Acw2-5 Acm5-7 Acw1 Acw11-12 Acm9 Acw6-7 Taurus Ac1-3 Acu3-5 A. c. muhtari A. c.wolteri A. c.cappadocica A. c. schmidtlerorum Ayas1-6 A. c. urmiana A. yassujica Fig. 1. Map showing the sampling localities of the specimens examined. Numbers refer to specimen codes given in the Table 1. The dashed black line shows the distribution of A. cappadocica. The shaded areas correspond to the subspecies distributions (Sindaco and Jeremcˇenko, 2008). The thick black line represents the ‘‘Anatolian Diagonal’’ which runs through northeast and central Turkish Anatolia (Nilson et al., 1990). Iraq, and West Iran (Arnold et al., 2007; Eiselt, 1979; Nilson et al., acting as a vicariant agent (Tchernov, 1992). The Taurus Mountains, 2003). It is unique among Lacertini in having clear single keels on the Bitlis-Pötürge Massif, the Zagros Mountains, the Anatolian Diag- scales beneath toes, a transparent window in the lower eyelid con- onal, the Central Anatolian Plateau, and the Central Anatolian Lake sisting of several black-edged scales, and variable scaling on the system acted as most obvious barriers (Eronen et al., 2009; Nilson side of the snout that may involve up to three postnasal and three et al., 1990; Popov et al., 2006; Rögl, 1999). The formation of the loreal scales and sometimes an additional scale between the rostral mountain chains in Anatolia can be traced back to the Tertiary, and the nostril (Arnold et al., 2007). when the northward movement of Europe resulted in the formation The first species (A. cappodocica) is polytypic and includes five of the Alps. The Central Anatolian lake system that is located be- subspecies [A. c. cappadocica (Werner, 1902), A. c. urmiana (Lantz tween the Taurus and the Black Sea Mountains, was also initially and Suchow, 1934), A. c. wolteri (Bird, 1936), A. c. muhtari (Eiselt, formed in that time and persisted cyclically until the end of the 1979), and A. c. schmidtlerorum (Eiselt, 1979)] with high protein Pliocene (Bilgin, 2011 and references therein). (blood-serum) differentiation (Ilgaz et al., 2010; Nilson et al., Severe climatic changes have also played a key role on the evo- 2003). On the other hand, A. yassujica with strongly keeled subdig- lutionary and biogeographical history of animals inhabiting this ital lamellae and eyelid with transparent window of several scales area, since climatic oscillations between significantly wetter and is a monotypic species. It differs from A. cappadocica in having a drier conditions have produced repeated habitat changes and peri- completely different color pattern, smaller size, fewer transverse odic modifications of major biota (Douady et al., 2003; Prentice ventral plate series, fewer dorsal, gular and collar scales, and and Jolly, 2000). The late Neogene represents a significant period smooth or obtusely keeled caudal scales (Nilson et al., 2003). in Cenozoic climatic history with major expansion of dry zones Anatolia, the region encapsulating most of the Apathya’s range and replacement of forests by woodlands and grasslands, occurring (Fig. 1) has a complicated geological history that has also left an im- particularly in the mid-latitudes in this time interval (as described print on the biogeography of many other vertebrate taxa, especially by Kornilios et al. (2012)). The cause(s) of this global aridification amphibians and reptiles (see Bilgin, 2011 for review; Kornilios et al., trend are not yet fully understood, although it is commonly be- 2012). Located in the Alpine–Himalayan Mountain belt between lieved that there is a general relation with global Cenozoic cooling, Eurasia, Africa and Arabia, Anatolia, its geomorphology is the result since atmospheric moisture content decreased with decreasing air of the collision of the Arabian and African plates with the European temperature (Kornilios et al., 2012). Due to their presumed limited plate, which promoted the closure of the Tethys Sea (Rögl, 1998). natural-dispersal capacities and temperature dependence, reptiles Due to its position and geological history, Anatolia has acted either are sensitive indicators of the palaeogeographical and palaeocli- as a bridge or as a barrier for species’ dispersal between Asia, matic events that have shaped their biogeographic history. Thus, Europe, and the Ethiopian region, providing a natural pathway or studying the patterns and process that
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