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Phylogeography of the Middle Eastern Tree Frogs (Hyla, Hylidae, Amphibia

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Phylogeography of the Middle Eastern Tree Frogs (Hyla, Hylidae, Amphibia Molecular Phylogenetics and Evolution 55 (2010) 1146–1166 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeography of the Middle Eastern tree frogs (Hyla, Hylidae, Amphibia) as inferred from nuclear and mitochondrial DNA variation, with a description of a new species Václav Gvozˇdík a,b,c,*, Jirˇí Moravec b, Cornelya Klütsch d,e, Petr Kotlík a a Department of Vertebrate Evolutionary Biology and Genetics, Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, 277 21 Libeˇchov, Czech Republic b Department of Zoology, National Museum, 115 79 Prague, Czech Republic c Faculty of Science, Charles University, Department of Zoology, Vinicˇná 7, 128 44 Prague, Czech Republic d Zoologisches Forschungsinstitut und Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany e KTH-Royal Institute of Technology, Gene Technology, Roslagstullsbacken 21, 10691 Stockholm, Sweden article info abstract Article history: Evolutionary relationships of the tree frogs from the Middle East and the demographic histories of their Received 25 September 2009 populations were studied using a combination of mitochondrial and nuclear genes. Hyla savignyi and Revised 13 February 2010 neighboring populations of H. orientalis (former eastern populations of H. arborea) were the main focus Accepted 10 March 2010 taxa. Within H. savignyi, a deep phylogenetic divergence dated about 8.4 Ma was discovered. Southern Available online 20 March 2010 populations from Yemen, Jordan, southern Syria and extreme north-eastern Israel are hereby described as a new species, H. felixarabica sp. nov. Our study points to a biogeographic connection of the south-wes- Keywords: tern Arabian Peninsula and southern Levant and to the importance of the Dead Sea Rift as a historical bar- Hyla savignyi rier geographically separating the new species from H. savignyi. Major genetic breaks revealed within Hyla felixarabica sp. nov. Hyla orientalis species (H. felixarabica: Yemen vs. Jordan–Syria; H. savignyi sensu stricto: Levant vs. Turkey–Iran) are Hyla arborea probably connected to climate changes during the Plio–Pleistocene boundary, while the finer phylogeo- DNA graphic structuring probably resulted from the Quaternary climate oscillations. The Cypriote population 12S and 16S rRNA of H. savignyi originated from southern Anatolia relatively recently. Hyla orientalis from the southern Rhodopsin Black Sea region seems to be genetically quite uniform, although two phylogeographic units with western Tyrosinase Turkish and Caucasus–Caspian affinities might be detected. Hyla savignyi and H. orientalis carry signals of Biogeography population expansions dated to the middle to late Pleistocene, while populations of H. felixarabica seem Demography to have rather been constant in size, which might indicate more stable climatic conditions in the southern Taxonomy regions during the Quaternary. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction et al., 2007; Plötner et al., 2001; Prager et al., 1998; Stöck et al., 2006). Most of the available phylogeographic studies focused only The Middle East constitutes an important zoogeographic region on the situation in Anatolia and/or Transcaucasia (Bohlen et al., on the crossroads of Palearctic, Oriental and Afrotropic ecozones. 2006; Dubey et al., 2007b; Furman et al., 2009; Gündüz et al., Some areas within this region, such as the Mediterranean, Cauca- 2005, 2007; Hrbek et al., 2002, 2004; Tarkhnishvili et al., 2000, sus Mountains or southern Caspian Sea coast, served during the 2001; Veith et al., 2003, 2008; Weisrock et al., 2001). The studies Pleistocene climatic cycles as important refugia for predominantly have shown different phylogeographic patterns in different taxa, European biota (e.g. Hewitt, 1999), while other areas, such as cen- although some general patterns have been found. The first group tral Anatolia or Gulf of Persia provided refugia for strictly Middle consists of taxa that are endemic to some smaller part of the Mid- Eastern species (e.g. Fritz et al., 2008). However, up to now, few dle East (usually Anatolia), although they possess a high genetic phylogeographic vertebrate studies covering a substantial part of diversity [e.g. fishes (Bohlen et al., 2006; Hrbek et al., 2002, the Middle East have been published (e.g. Dubey et al., 2007a; Fritz 2004), salamanders (Tarkhnishvili et al., 2000; Veith et al., 2008; et al., 2007, 2008; Kapli et al., 2008; Kyriazi et al., 2008; Macholán Weisrock et al., 2001), rodents (Gündüz et al., 2007)]. Another group includes widespread taxa that form two or more lineages covering larger geographic areas [e.g. water and brown frogs (Plöt- * Corresponding author at: Department of Vertebrate Evolutionary Biology and ner et al., 2001; Plötner, 2005; Tarkhnishvili et al., 2001; Veith Genetics, Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, 277 21 Libeˇchov, Czech Republic. Fax: +420 315 639 510. et al., 2003), tortoises and terrapins (Fritz et al., 2007, 2008, E-mail address: [email protected] (V. Gvozˇdík). 2009), lizards (Kapli et al., 2008; Kyriazi et al., 2008), shrews 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.03.015 V. Gvozˇdík et al. / Molecular Phylogenetics and Evolution 55 (2010) 1146–1166 1147 (Dubey et al., 2007a,b), mice (Macholán et al., 2007), bats (Furman here sequences of multiple mitochondrial (12S rRNA and 16S et al., 2009)], or a single widespread lineage but with substantial rRNA) and nuclear genes (rhodopsin and tyrosinase) as well as a genetic variation, as was documented in green toads (Stöck et al., dense sampling covering the distributions of tree frogs in the Mid- 2006). These studies often related the deepest genetic divergences dle East (Supplementary data; Fig. S1, Table S1). Although our to the plate tectonics in the Miocene and/or associated geological study builds on earlier works (Gvozˇdík et al., 2007a; Stöck et al., events, such as the Messinian salinity crisis, and such divergences 2008), only with our new approach, based on a combination of ge- are considered interspecific, forming cryptic species complexes. netic, bioacoustic and morphological analyses, the data set be- Shallower, younger genetic structuring is then typically inter- comes adequate to provide a compelling description of the preted as a result of climatic oscillations (and associated aridifica- evolutionary history and molecular systematics of tree frogs in tion) during the Pliocene or the Quaternary. Furthermore, in some the Middle East. Our goals are to (i) reveal the number, phyloge- species present phylogeographic patterns may have also been netic relationships and geographic distribution of evolutionary lin- influenced by human activity, such as continental or overseas eages; (ii) propose historical biogeography and demography transport, as inferred for commensal mice (Gündüz et al., 2005), scenarios to accommodate the genetic variation observed among shrews (Dubey et al., 2007a), or even skinks (Kornilios et al., 2010). and within lineages and (iii) evaluate the validity and revise Tree frogs of the genus Hyla are small, semiaquatic vertebrates, boundaries of the currently recognized taxa. widely distributed throughout the Middle Eastern region. For their reproduction, tree frogs are dependent on open waters (e.g. pools, springs, artificial water reservoirs), with rather warm-climate pref- 2. Materials and methods erence. Their distribution in this relatively arid and topographically variable region is therefore limited by the availability of such hab- 2.1. Samples for genetic study itats. Taking into account their relatively low mobility (apart from possible accidental transport by human; Recuero et al., 2007), high Tissue samples (H. savignyi sensu lato (s.l.): n = 150, 66 locali- and cold mountain ridges of Anatolia, Kurdistan or Iranian High- ties; H. orientalis: n = 44, 19 localities) were obtained from museum lands, or deserts in central Iran, eastern Levant or most of Arabian voucher specimens (National Museum, Prague, Czech Rep.). In Peninsula might form effective barriers to dispersal of tree frogs. addition, toe clips, tadpole tail tips and oral swabs were collected These attributes make tree frogs an excellent model for a study in the field. Additional sequences of three individuals of H. savignyi of phylogeography and biogeography of the Middle East. s.l. (yielding one additional locality) and an outgroup species H. Systematics and taxonomy of tree frog species occurring in the japonica were taken from GenBank (Yemen: AY843665, Middle East, in particular Asia Minor, Transcaucasia, Iranian Pla- AY844654, AY844107, Faivovich et al., 2005; Syria: EF566954, teau, Mesopotamia, Levant, Cyprus and Arabian Peninsula, have Moriarty Lemmon et al., 2007 and DQ055843, Smith et al., 2005; not been sufficiently resolved yet. Therefore, it remains unclear if and Japan: AY843633, AY844615, AY844078, Faivovich et al., there are three or four species of the genus Hyla present in the area. 2005). Another outgroup species, H. meridionalis Boettger, 1874, a One species, Hyla savignyi Audouin, 1827 [‘‘1809”], occurs in south- specimen from Tenerife Island, the type locality, was sequenced ern and eastern Asia Minor, eastern Transcaucasia, northern and by us. More details might be found in Supplementary data western Iran, Iraq, Levant, extreme north-eastern Sinai, and there (Fig. S1, Table S1).
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