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A Molecular Phylogeny of the Eastern Group of Ocellated Lizard Genus Timon (Sauria: Lacertidae) Based on Mitochondrial and Nuclear DNA Sequences

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A Molecular Phylogeny of the Eastern Group of Ocellated Lizard Genus Timon (Sauria: Lacertidae) Based on Mitochondrial and Nuclear DNA Sequences Amphibia-Reptilia 33 (2012): 1-10 A molecular phylogeny of the eastern group of ocellated lizard genus Timon (Sauria: Lacertidae) based on mitochondrial and nuclear DNA sequences Faraham Ahmadzadeh1,2,∗, Miguel Angel Carretero3, D. James Harris3, Ana Perera3, Wolfgang Böhme2 Abstract. Timon, a small genus of lacertid lizards, includes four species distributed in two separate ranges in the western and eastern part of the Mediterranean Basin. Phylogenetic relationships between the two groups have not been resolved, and the taxonomic situation of the two subspecies of the eastern representative of the genus, Timon princeps, is not clear. To address these questions, partial DNA sequences of two nuclear (β-fibrinogen intron 7 and C-mos) and three mitochondrial (cytochrome b, 12S rRNA and 16S rRNA) genes were analyzed. Based on the high genetic distance between the two subspecies of T. princeps we promote their taxonomic status to full species, Timon princeps and Timon kurdistanicus. Divergence time estimates based on other lacertid species suggest that the separation of the green (Lacerta) and ocellated (Timon) lizards took place around 12 My ago, and that the Eastern group underwent speciation around 4-5 my ago, perhaps associated with the uplifting of the Zagros mountains. As expected given this ancient divergence and complex paleogeography, considerable levels of genetic diversity are recovered within both taxa, with geographically close individuals showing very divergent haplotypes. Keywords: lacertid lizards, mtDNA, nDNA, phylogeny, Timon kurdistanicus, Timon princeps. Introduction into several small but generally monophyletic units (Arnold et al., 2007). However, the mono- The evolutionary history of lacertid lizards has phyly of some units (such as Algyroides)was been the subject of various investigations (Lutz not tested, while others (such as Timon)were and Mayer, 1984; Arnold, 1989; Mayer and not supported. Bischoff, 1996; Arribas, 1997; Fu et al., 1997; Timon as currently accepted is a small genus Harris et al., 1998; Fu, 2000; Carranza et al., comprising four species of large ocellated 2004; Godinho et al., 2005; Arnold et al., lizards, Timon princeps (Blanford, 1874), Ti- 2007; Pavlicev and Mayer, 2009). However, mon lepidus (Daudin, 1802), Timon tangitanus most of these attempts to reconstruct the phy- (Boulenger, 1889) and Timon pater (Lataste, logeny of lacertids resulted in unresolved bush- 1880) distributed across two main geographic like topologies (Pavlicev and Mayer, 2009). In regions: the eastern and the western Mediter- one of the most recent efforts, based on mor- ranean. The Timon lepidus group, consisting of phological and molecular characterization, the T. lepidus (with three recognized subspecies, but then polyphyletic genus Lacerta s. l. was split see Miraldo et al., 2011), T. pater and T. tangi- tanus, occupies the western part of the Mediter- 1 - Department of Biodiversity and Ecosystem Manage- ranean basin including the Iberian Peninsula, ment, Environmental Sciences Research Institute, Sha- southern France and northwestern Italy in Eu- hid Beheshti University, G.C., Evin, Tehran, Iran 2 - Zoologisches Forschungsmuseum Alexander Koenig, rope and Morocco, Algeria and Tunisia in North Adenauerallee 160, 53113 Bonn, Germany Africa (Arnold et al., 2007; Paulo et al., 2008; 3 - CIBIO, Centro de Investigação em Biodiversidade e Perera and Harris, 2010; Miraldo, 2011). On Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal the other hand, Timon princeps is distributed ∗Corresponding author; e-mail address: in eastern Turkey and in Iran from Kurdistan [email protected] through western Zagros to Fars Province (An- © Koninklijke Brill NV, Leiden, 2012. DOI:10.1163/156853811X619718 2 F. Ahmadzadeh et al. derson, 1999; Ilgaz and Kumlutas, 2008; Sin- Materials and methods daco and Jeremcenko, 2008), and includes two In total, 16 samples of T. princeps covering all the distri- currently recognized subspecies (Eiselt, 1968, bution range of the species were analysed. Specimen codes 1969, 1970; Anderson, 1999). used in this study and their respective locations can be found in table 1. Total genomic DNA from each individual was These eastern and western species appear to extracted from tail tips using standard saline methods (Sam- be related on the basis of albumin immunol- brook et al., 1989). Polymerase chain reaction (PCR) am- ogy (Lutz and Mayer, 1984) and some mor- plifications were performed for all samples using three dif- ferent mitochondrial DNA fragments (cytochrome b, 16S phological features (Eiselt, 1968, 1969). Har- rRNA and 12S rRNA). Additionally, in order to investigate ris et al. (1998), based on mitochondrial DNA the phylogenetic relationships between Timon and other lac- sequences showed that the two discrete groups ertids, two nuclear DNA fragments (β-fibrinogen and C- mos) were amplified for two individuals of each recog- are monophyletic. On the other hand, Arnold et nized subspecies (T. p. princeps and T. p. kurdistanicus). al. (2007), despite recognizing Timon as a full The amplification and sequencing of three mtDNA gene genus, did not recover the monophyly of the fragments was performed using the primers GluDG/Peil T. princeps Ti- (modified from Palumbi et al., 1991 and Engstrom et al., group, with unrelated to other 2007), 16SL/16SH (Palumbi et al., 1991), and 12Sa/12Sb mon species albeit without strong support. None (Kocher et al., 1989). For the amplification of intron 7 of of the available DNA studies provide a fully re- the β-fibrinogen and the C-mos gene, the primers FIB-BI7U solved hypothesis of relationships between the and FIB-BI7L (Prychitko and Moore, 1997), and LCS1 and LCS2 (Godinho et al., 2005) were used, respectively. These two main groups, although “western” Timon five sets of primers amplified regions of approximately 950, species are usually found to be the sister taxa 550, 450, 700 and 550 base pairs, respectively. of Lacerta s. str. (Harris et al., 1998; Fu, 2000; In all cases, PCR mix was carried out in a 25 μltotal volume, containing 2.5 μl reaction Buffer, 1.5 mM of Arnold et al., 2007). Regarding the variation MgCl2, 0.5 mM each dNTP, 0.5 mM each primer, 0.1U Taq within each group, several recent studies inves- DNA polymerase (Invitrogen) and approximately 100 ng of template DNA with the following conditions: an initial cycle tigated the phylogeographic patterns within the ◦ ◦ of 92 for2min,followedby35cyclesof92 C for 30 s, T. lepidus group (Paulo et al., 2001, 2008; Per- 50◦ for 40 s (54◦ for nuclear genes) and 72◦ for 45 s, and a era and Harris, 2010; Miraldo et al., 2011). Con- final cycle of 72◦ for 5 min. All amplified fragments were cerning the eastern group, although the mor- sequenced by a commercial company (Macrogen, Korea). Sequences were imported to Bioedit (Hall, 1999) where phology of T. princeps has been discussed ex- they were first aligned using ClustalW with default param- tensively by Eiselt (1968, 1969), its genetic vari- eters and then adjusted by hand. Sequences are available in ation and phylogeographic patterns remain un- GenBank (table 1). In order to investigate the relationships of the genus Ti- known. This author recognizes the existence of mon with other lacertids sequences, a phylogenetic analy- two different subspecies: T. princeps kurdistan- sis using the five amplified fragments (both mtDNA and icus and T. p. princeps. Both subspecies are sep- nDNA) was performed. Separate and combined analyses were performed using MP. Conflict between partitions was arated on the basis of pholidotic and meristic assessed using the qualitative evaluation of Wiens (1998). characteristics, but as far as we know, no genetic Since there was no strong conflict between gene regions, data regarding the validation of these two mor- concatenated analyses were performed. All genes were con- catenated resulting in a final fragment of 2713 bp. From the phologically differentiated groups exist. GenBank database, previously published sequences of the Therefore, the three main objectives of this same genes belonging to five species of Lacerta (L. agilis, study are: 1) what are the phylogenetic relation- L. pamphylica, L. schreiberi, L. viridis, L. strigata), as well as three species of the western group of Timon (T. lepidus, ships between the eastern and western groups? T. pater and T. tanginatus – Godinho et al., 2005; Paulo et In particular, are “western” Timon more closely al., 2008) were added to our analysis (table 1). Due to their related to Lacerta s. str.? 2) what is the level of shorter length, only 2084 bp (350 bp 12s rRNA, 420 bp 16 rRNA, 306 bp cytochrome b, 317 bp C-mos, 691 bp β- genetic variability between the two subspecies fibrinogen) fragments could be included in the final anal- of T. princeps? and finally, 3) what shaped ysis. Archaeolacerta bedriagae was included as the closest the current biogeographic pattern of the eastern available outgroup (Pavlicev and Mayer, 2009; Savli, unpub. data). populations, and when did they start to diverge Sequences were analysed using Bayesian inference (BI), and how? maximum-parsimony (MP) and maximum likelihood (ML) Molecular phylogeny of Table 1. List of samples analyzed, sampling localities, origin of the samples and GenBank accession numbers for the samples included in this study. Species Code Locality Origin GenBank accession numbers (12S, 16S, cytb, C-mos, β-fib) Timon Timon princeps kurdistanicus DB6235 Iran, Kurdistan, Sarv Abad This study JQ425790 JQ425806 JQ425830 – – Timon
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