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Zoology in the Middle East

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Phylogeny and biogeography of Arabianpopulations of the Persian Horned ViperPseudocerastes persicus (Duméril, Bibron &Duméril, 1854)

Philip de Pous, Marc Simó-Riudalbas, Johannes Els, Sithum Jayasinghe, FelixAmat & Salvador Carranza

To cite this article: Philip de Pous, Marc Simó-Riudalbas, Johannes Els, Sithum Jayasinghe, FelixAmat & Salvador Carranza (2016): Phylogeny and biogeography of Arabian populations of thePersian Horned Viper Pseudocerastes persicus (Duméril, Bibron & Duméril, 1854), Zoology inthe Middle East, DOI: 10.1080/09397140.2016.1202896

To link to this article: http://dx.doi.org/10.1080/09397140.2016.1202896

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Zoology in the Middle East, 2016 http://dx.doi.org/10.1080/09397140.2016.1202896

*Corresponding author. Email: salvador.carranza@ibe.upf-csic.es

© 2016 Taylor & Francis

Phylogeny and biogeography of Arabian populations of the Persian Horned Viper Pseudocerastes persicus (Duméril,

Bibron & Duméril, 1854) Philip de Pousa,b, Marc Simó-Riudalbasa, Johannes Elsc, Sithum Jayasinghec,

Felix Amatd and Salvador Carranzaa,*

aInstitute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain; bDepartament de Producció Animal, Faculty of Life Sciences and Engineering, Universitat de Lleida, Lleida, Spain; cBreeding Centre for Endangered Arabian Wildlife, Environment and

Protected Areas Authority, Sharjah, United Arab Emirates; dÀrea d‘Herpetologia, Museu de Granollers-Ciències Naturals, Granollers, Catalonia, Spain

(Received 15 November 2015; accepted 29 May 2016)

The Persian Horned Viper (Pseudocerastes persicus) is distributed from northeast Iraq through the Iranian Plateau to western Pakistan with isolated populations in the Hajar Mountains of south-eastern Arabia. Like the other members of the genus Pseu-docerastes, P. persicus is a sit-and-wait ambush feeder with low vagility, a character-istic that often results in high levels of population differentiation. In order to clarify the level of genetic variability, phylogenetic relationships, and biogeography of the Arabian populations of P. persicus we sequenced 597 base pairs of the mitochondrial cytochrome b of four individuals from the Hajar Mountains in south-eastern Arabia and inferred their phylogenetic relationships including 10 samples of P. persicus from Iran and Pakistan, four P. urarachnoides and one P. fieldi downloaded from GenBank. The four Arabian samples are genetically very similar in the gene frag-ment analysed and are phylogenetically very closely related to populations of P. per-sicus from coastal south Iran. Biogeographically, it appears that colonisation of the Hajar Mountains by P. persicus took place from Iran very recently, most probably during the last glaciation, when most of the Persian Gulf was above sea level and did not represent a barrier for dispersal.

Keywords: Pseudocerastes persicus; Arabia; cytochrome b; Viperidae; Hajar Moun-tains; species distribution

Introduction The genus Pseudocerastes Boulenger, 1896 consists of three species that are distributed in Western Asia and the Middle East: Pseudocerastes fieldi Schmidt, 1930, P. persicus (Duméril, Bibron & Duméril, 1854), and P. urarachnoides Bostanchi, Anderson, Kami & Papenfuss, 2006. Although some authors have considered P. fieldi as a subspecies of P. persicus (e.g. Leviton, Anderson, Adler, & Minton, 1992), it is now generally ac-cepted as a full species based on morphology (Bostanchi, Anderson, Kami, & Pa-penfuss, 2006; Fathinia & Rastegar-Pouyani, 2010), genetics (Lenk, Kalyabina, Wink, & Joger, 2001; Pyron, Burbrink, & Wiens, 2013) and venom differences (Bdolah, 1986 [although differences in venom composition were found, no taxonomic changes were suggested]; Ali et al., 2015). In fact, a recent study using a fragment of the cytochrome b mitochondrial gene indicates that P. fieldi is the sister taxon to a clade formed by

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P. urarachnoides and P. persicus (Fathinia, Rastegar-Pouyani, Rastegar-Pouyani, Toodeh-Dehghan, & Rajabizadeh, 2014), confirming the specific status of the three forms.

The distribution area of the Persian Horned Viper (P. persicus) extends from north-east Iraq through the Iranian Plateau to western Pakistan with isolated populations in southeastern Arabia (Oman and UAE; Fathinia & Rastegar-Puyiani, 2010; Sindaco et al., 2013). Arnold and Gallagher (1977) first reported the presence of the species in Oman and provided morphological data on one male and one female from the Jebel Akhdar (Hajar Mountains). Subsequently, Gasperetti (1988), Feulner (1999, 2014), van der Kooij (2001), Cunningham (2002) and Grossmann, Kowalski, Zwanzig, and Zilger (2012) provided additional records and substantially extended the known distribution of P. persicus in Oman and the UAE, which seems to favour rugged and rocky areas above 800 metres that are seldom visited by humans (see Fig. 1 and Supplementary Fig. S1). Despite these new records, P. persicus still ranks as one of the rarest reptiles of the Hajar Mountains (Gardner, 2013) and very little is known about its systematics, distri-bution, ecology and conservation in this region. It is categorized in the Arabian Peninsu-la as regionally vulnerable by the IUCN (Cox, Mallon, Bowles, Els, & Tognelli, 2012). Habitat destruction due to development and quarrying has been identified as a threat to the species within the region at present and in the foreseeing future.

Like the other members of the genus, Pseudocerastes persicus is a sit-and-wait am-bush predator with low dispersal capacity, a characteristic that often results in high levels of population differentiation, something that has recently been corroborated by the presence of substantial genetic variability at the mitochondrial DNA level in the Iranian populations (Fathinia et al., 2014). The Arabian populations of P. persicus are distributed across the Hajar Mountains in the extreme southeastern Arabia and are there-fore isolated from the Iranian populations by a sea barrier. Despite the obvious interest from a systematic and biogeographic point of view, the lack of samples of Arabian P. persicus for genetic studies have prevented any phylogenetic studies that could clarify the origin and taxonomy of these isolated populations. Recent molecular studies indicate that the diversity of reptiles in Arabia and especially in the Hajar Mountains of Oman and UAE is much higher than it was previously thought, with some species showing very high levels of genetic variability even across very short distances (Papenfuss et al., 2009; Carranza & Arnold, 2012; Šmíd et al., 2013; Badiane et al., 2014; Metallinou et al., 2015; de Pous et al., 2016). Besides its relevance from a biodiversity point of view, to know the level of genetic differentiation and to have a good systematic knowledge that correctly reflects the phylogenetic relationships have important implications in venomous snakes. Venom composition can vary even between closely related species and therefore a robust taxonomic framework is highly relevant for toxinological re-search and the production and administration of the correct antivenom (see e.g. Ali et al., 2015).

In this work we use DNA sequences of the cytochrome b mitochondrial gene from four individuals of P. persicus from the Hajar Mountains to infer the phylogenetic rela-tionships and biogeography of the enigmatic Arabian population of P. persicus.

Material and Methods Material. The four Arabian specimens of P. persicus included in the phylogenetic analyses were collected by the authors during fieldwork expeditions in Oman in May 2013 and the UAE in October 2015 (see Figure 1 and Supplementary Figures S1 and S2): (1) On 10 May 2013 (23.00°N, 57.70°E, 1589 m a.s.l.) a fresh road-killed specimen was found by P.P. in a steep curve while descending the road from Saiq to Birkat Al Mouz (Appendix 2A); (2) On 21 May 2013 a live specimen was collected by S.C. M.S. and F.A. on Jebel Kawr (23.14°N, 57.03°E, 2270 m a.s.l.) while escaping under a medium sized stone in a rocky area almost devoid of vegetation

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(Appendix 2B); (3) On 22 May 2013 a specimen was collected close to Jebel Shams by P.P., S.C., M.S. and F.A., about 5 km west of the village of Karb (23.28°N, 57.16°E, 2116 m a.s.l.). The specimen was basking in the afternoon sun while partly hidden in the crevice of a large rock (Appendix 2C); (4) On 17 October 2015 a live specimen was collected by J.E. and S.J. on the Hajar mountain range along the east coast of Sharjah, UAE (25.03°N, 56.21°E, 815 m a.s.l.), very close to a locality previously published by Feulner (2014). The habitat was nearly absent of vege-tation and rocky and the animal was in an ambush position slightly cratered in the soft substrate between smaller rocks. Sampling, DNA extraction and sequencing. A total of 21 individuals were included in the phy-logenetic analyses: 4 Pseudocerastes urarachnoides, 14 P. persicus and one specimen of P. fieldi. Two individuals of Eristichophis macmahoni were used as outgroups based on published evi-dence (Pyron et al., 2013). A list of all specimens included in the molecular study with their taxo-nomic identification, sample codes, voucher references, geographical distribution data and Gen-Bank accession numbers is presented in Supplementary Table 1. For the four new samples of P. persicus from Arabia, genomic DNA was extracted from ethanol-preserved tissue samples using the SpeedTools Tissue DNA Extraction kit (Biotools, Madrid, Spain). Partial sequences of the mitochondrial cytochrome b (cytb) were PCR-amplified and sequenced in both directions using primers L14910 5´-GAC-CTG-TGA-TMT-GAA-AAC-CAY-CGT-TGT-3´ and H16064 5´-CTT-TGG-TTT-ACA-AGA-ACA-ATG-CTT-TA-3’ from Burbrink, Lawson, and Slowinski (2000) using 40 PCR cycles with the following conditions: 94° 40'', 46° 30'', 72° 1'. Geneious v. R6 (Biomatters Ltd.) was used for assembling and editing manually the chromatographs. The cytb coding fragments were translated into amino acids and no stop codons were observed. DNA sequences were aligned using MAFFT v.7 (Katoh & Standley, 2013) applying parameters by default (Auto strategy, Gap opening penalty: 1.53, Offset value: 0.0). Uncorrected p-distances with complete deletion were estimated for the cytb mitochondrial fragments using MEGA v.5 (Tamura et al., 2011). The level of substitution saturation was assessed by using the substitution saturation test of the program package DAMBE v. 5.3.46 (Xia, 2013). Phylogenetic analyses. Phylogenetic analyses were performed using maximum likelihood (ML) and Bayesian inference (BI) methods. The best-fitting model was inferred using jModeltest v.2.1.3 (Guindon & Gascuel, 2003; Darriba, Taboada, Doallo, & Posada, 2012) under the Akaike Information Criterion (AIC) (Akaike, 1973). ML analyses were performed in RAxML v.7.0.3 (Stamatakis, 2006). A GTR+G model of sequence evolution was used with parameters estimated independently for each partition and the reliability of the ML tree was assessed by bootstrap analysis (Felsenstein, 1985) including 1000 replications. Bayesian analyses were performed with BEAST v.1.7.5 (Drummond & Rambaut, 2007) using the same dataset used in the ML analysis but without outgroups. Analyses were run twice for 1x107 generations with a sampling frequency of 5000 generations. Models and prior specifications applied were as follows (otherwise by de-fault): model of sequence evolution TrN+I; Yule process of speciation; random starting tree; fix mean rate of molecular clock model to 1. Posterior trace plots and effective sample sizes (ESS) of the runs were monitored in Tracer v1.5 (Rambaut & Drummond, 2009) to ensure convergence. The results of the individual runs were combined in LogCombiner discarding 10% of the samples and the ultrametric tree was produced with TreeAnnotator (both provided with the BEAST pack-age). Nodes in the phylogenies were considered strongly supported if they received ML bootstrap values ≥70% and posterior probability (pp) support values ≥0.95 (Huelsenbeck & Rannala, 2004; Wilcox, Zwickl, Heath, & Hillis, 2002).

Results The dataset used for the phylogenetic analyses consisted of an alignment of 597 base pairs (bp) of cytb, of which 117 were variable and 60 were parsimony-informative. Ingroup sequences do not present substitution saturation (data not shown). The results of the BI and ML analyses of the genus Pseudocerastes are presented in Figure 2. The two trees were very similar, differing only in the position of P. persicus KF314711 (sister taxon to the clade formed by coastal south Iran and Omani P. persicus popula-tions in the ML tree) and in the branching order of the two coastal south Iran

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Figure 1. Distribution of Pseudocerastes persicus in the Arabian Peninsula with all known dis-tribution records (no. 1–4 show the new samples). The map also shows the two coastal south Iran populations of P. persicus (Saraj and Bandar-e-Abbas) sister group to the Omani populations in the phylogenetic analyses. populations (KF314712 sister taxon to an unsupported clade formed by KF314713 and the Arabian populations in the ML tree). Pseudocerastes fieldi is sister to a clade formed by P. urarachnoides and P. persicus, although this latter clade is only supported by the BI analysis. The three Omani specimens sequenced for this study are genetically identical in the mitochondrial cytb gene and they differ by only 1 mutation from the UAE specimen (uncorrected genetic distance of 0.2%; see Supplementary Table S2). In the BI phylogenetic tree from Figure 2 the Arabian specimens branch as a sister group to P. persicus from Saraj and Bandar-e-Abbas in coastal south Iran (Figure 1). The uncorrected genetic distances for the cytb gene between the coastal south Iran and the Arabian populations range between 0.4%–1.2% (see Supplementary Table S2).

Apart from the four new records of P. persicus that correspond to the sequenced specimens included in the present work, other recent unpublished sightings of P. persi-cus personally communicated to J.E. include: Jebel Hafeet (one specimen found by a naturalist in late 2011, 24.06°N, 55.76°E, 683 m a.s.l., another one on 19 March 2016 found by Jacobo Reyes-Velasco and Joseph Manthey, 24.05°N, 55.79°E, 487 m a.s.l.); east coast of Hajar Mountains, Sharjah, UAE (one specimen found by a naturalist in early October 2015, 25.02°N, 56.20°E, 460 m a.s.l.).

Discussion The three records of Pseudocerastes persicus from Oman represent an interesting range extension to the eastern Jebel Akhdar and the isolated Jebel Kawr (see Supplementary Figure S1). The species likely has a continuous range in the higher elevations from the

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Figure 2. BI tree of 19 Pseudocerastes based on partial sequences of the mitochondrial cyto-chrome b gene. Black dots indicate posterior probability values ≥0.95 in the Bayesian analysis and bootstrap values ≥70% in the ML analysis are shown next to the nodes. The tree was rooted using two specimens of Eristichophis macmahoni (not included in the figure). Each tip of the phylogenetic tree is labelled with the species name followed by the GenBank accession number, with the only exception of the three new specimens from Oman that are labelled with the species name followed by the specimen code and locality number according to Figure 1 and Supplemen-tary Table 1. Abbreviations: M-P-D, Maybod-Pakistan-Damghan specimens from Fathinia et al. (2014). Ru’us al-Jibal in the Musandam Peninsula to Jebel Qahwan in the extreme eastern Hajar Mountains. As mentioned by Cunningham (2002), this species could be limited to the higher elevations due to competition with Echis carinatus and E. omanensis at lower elevations, the latter being much larger and aggressive than P. persicus (Gardner, 2013; pers. obs.). As an Asian member of the genus Pseudocerastes, P. persicus probably tolerates slightly lower temperatures than the mainly Arabian and African carpet vipers of the genus Echis (Arnold, Robinson, & Carranza, 2009) and can therefore adapt better to the higher elevations of the Hajar Mountains. Nevertheless, some recent records situate P. persicus at altitudes of 460-487 m a.s.l., contradicting Egan (2007), who sug-gested that the species is only found above 600 m a.s.l.. Field surveys carried out by J.E. and S.J. around the Hajar mountain range along the east coast of Sharjah, UAE has confirmed that P. persicus lives at close proximity to other snake species including Echis omanensis, Telescopus dhara and Psammophis shokari, although E. omanensis was present in lower densities compared to lower altitude localities with permanent water where the species is abundant predating on Sclerophrys arabica (J.E. and S.J., pers. observ.). In view of the new data presented here, further research is needed on the possible competition between P. persicus and E. omanensis across their distribution ranges in the Hajar Mountains.

The phylogenetic relationships agree with the current taxonomy of Pseudocerastes and confirm that the Arabian populations belong to P. persicus (Uetz, 2015). Judged by

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the low level of genetic divergence between the coastal south Iran and Arabian popula-tions and the extremely low genetic variability between the four Arabian specimens (one single mutation in 597 bp) we suggest that Arabia was colonised from Iran very recently and that the expansion across the Hajar Mountains occurred relatively quickly. Colonisation could have happened by transmarine dispersal across the Persian or Oman Gulfs or directly by land dispersal across the Persian Gulf during the last glaciations. Water depths in the Persian Gulf do not generally exceed 100 m and the average depth is only about 35 m, thus it has been widely recognised that most of the Gulf has been above sea level during glacial time (Lambeck, 1996). Evidence suggests that until the Strait of Hormuz opened up as a narrow waterway approximately 14,000 years ago, the Persian Gulf was free of marine influence and continued like that until the flooding phase that reached the present shorelines 6,000 years ago (Lambeck, 1996). The deep basin of up to 3,400 m existing in the Gulf of Oman prevented its drainage even during the peak of the glaciations and therefore colonization across this area could have only been by transmarine colonisation.

Acknowledgements The Omani field work was made with the Permit nº 13/2013 of the General Director of Nature Conservation of the Ministry of Environment & Climate Affairs (MECA) of the Sultanate of Oman. We would like to thank Saleh Naghmush Al Saadi, Mohammed Juma Al Shariani, Thuraya Al Sariri, Ali Amer Al Kiyumi, and other members from MECA for their help and sup-port. We would also like to thank His Highness Sheikh Dr Sultan bin Mohammed Al Qasimi, Supreme Council Member and Ruler of Sharjah, Ms. Hana Al Suwaidi (Chairperson of the Envi-ronment and Protected Areas Authority, Sharjah) and Mr Paul Vercammen (Operations Manager, Breeding Centre for Endangered Arabian Wildlife) for their support. SC and MSR are members of the Grup de Recerca Emergent of the Generalitat de Catalunya: 2009SGR1462.

Funding This work was supported by the Ministerio de Economía y Competitividad (co-funded by FED-ER, EU) under grant CGL2012-36970; Ministry of Environment and Climate Affairs of the Sul-tanate of Oman under grant MECA-22412027 “Field study for the conservation of the reptiles of Oman”. PdP was funded by a FI-DGR grant (2013FI_B1 00110) from the Generalitat de Catalu-nya, Spain (2013FI_B1 00110) and MSR is funded by a FPI grant from the Ministerio de Economía y Competitividad, Spain (BES-2013-064248).

Disclosure Statement No potential conflict of interest was reported by the authors.

Supplementary Material Supplementary figures and tables are available via the “Supplementary” tab on the articles online tab (http://dx.doi.org/10.1080/09397140.2016.1202896).

References Akaike, H. (1973): Information theory and an extension of the maximum likelihood principle. Pp.

267–281. In B. N. Petrov & F. Csaki (Eds.), Information Theory and an Extension of the Maximum Likelihood Principle. Budapest: Akademiai Kiado.

Ali, S. A., Jackson, T. N., Casewell, N. R., Low, D. H., Rossi, S., Baumann, K., Fathinia, B., Visser, J., Nouwens, A., Hendrikx, I., Jones, A., Undheim, E. A., & Fry, B. G. (2015): Ex-treme venom variation in Middle Eastern vipers: A proteomics comparison of Eristicophis

Dow

nloa

ded

by [

81.6

1.17

4.21

6] a

t 14:

20 2

7 Ju

ne 2

016

Zoology in the Middle East 7

macmahonii, Pseudocerastes fieldi and Pseudocerastes persicus. Journal of Proteomics, 116, 106–113.

Arnold, E. N., & Gallagher, M. D. (1977): Reptiles and amphibians from the mountains of north-ern Oman with special reference to the Jebel Akhdar region. Journal of Oman Studies, Spe-cial Report, 1, 59–80.

Arnold, N. E., Robinson, M. D., & Carranza, S. (2009): A preliminary analysis of phylogenetic relationships and biogeography of the dangerously venomous Carpet Vipers, Echis (Squama-ta, Serpentes, Viperidae) based on mitochondrial DNA sequences. Amphibia-Reptilia, 30, 273–282.

Badiane, A., Garcia-Porta, J., Červenka, J., Kratochvíl, L., Sindaco, R., Robinson, M. D., Mo-rales, H., … Carranza, S. (2014): Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris. Zootaxa, 3835, 33–58.

Bdolah, A. (1986): Comparison of venoms from two subspecies of the false horned viper (Pseu-docerastes persicus). Toxicon, 24, 726–729.

Bostanchi, H., Anderson, S. C., Kami, H. G., & Papenfuss, T. J. (2006): A new species of Pseu-docerastes with elaborate tail ornamentation from Western Iran (Squamata: Viperidae). Pro-ceedings of the California Academy of Sciences, 57, 443–450.

Burbrink, F. T., Lawson, R., & Slowinski, J. B. (2000): Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies con-cept. Evolution, 54, 2107–2118.

Carranza, S., & Arnold, E. N. (2012): A review of the geckos of the genus Hemidactylus (Squa-mata: Gekkonidae) from Oman based on morphology, mitochondrial and nuclear data, with descriptions of eight new species. Zootaxa, 3378, 1–95.

Cox, N. A., Mallon, D., Bowles, P., Els, J., & Tognelli, M. F. (2012): The conservation status and distribution of reptiles of the Arabian Peninsula. Cambridge (UK) and Gland (Switzerland): IUCN and Environment and Protected Areas Authority of Sharjah.

Cunningham, P. L. (2002). Review of the False Horned Viper (Dumeril, Bibron & Dumeril, 1854) from the UAE and northern Oman, including a first record for Jebel Hafit. Tribulus: Journal of the Emirates Natural History Group, 12, 26-27.

Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). JModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772–772.

de Pous, P., Machado, L., Metallinou, M., Červenka, J., Kratochvíl, L., Paschou, N., Mazuch, T., Smid, J., Simó-Riudalbas, M., Sanuy, D., & Carranza, S. (2016): Taxonomy and biogeogra-phy of Bunopus spatalurus (Reptilia; Gekkonidae) from the Arabian Peninsula. Journal of Zoological Systematics and Evolutionary Research, 54, 67–81.

Drummond, A. J., & Rambaut, A. (2007): BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

Egan, D. (2007): Snakes of Arabia: a field guide to the snakes of the Arabian Peninsula and its shores. Dubai (UAE): Motivate.

Fathinia, B., & Rastegar-Pouyiani, N. (2010): On the species of Pseudocerastes (Ophidia: Viperi-dae) in Iran. Russian Journal of Herpetology, 16, 134–138.

Fathinia, B., Rastegar-Pouyani, N., Rastegar-Pouyani, E., Toodeh-Dehghan, F., & Rajabizadeh, M. (2014): Molecular systematics of the genus Pseudocerastes (Ophidia: Viperidae) based on the mitochondrial cytochrome b gene. Turkish Journal of Zoology, 38, 575–581.

Felsenstein, J. (1985): Confidence limits on phylogenies: an approach using the bootstrap. Evolu-tion, 39, 783–791.

Feulner, G. R. (1999): False Horned Viper. Gazelle, 16(11), 5. Feulner, G. R. (2014): The olive highlands: a unique “island” of biodiversity within the Hajar

Mountains of the United Arab Emirates. Tribulus, 22, 9–34. Gardner, A. S. (2013): The amphibians and reptiles of Oman and the UAE. Frankfurt a.m.: Edi-

tion Chimaira. Gasperetti, J. (1988): Snakes of Arabia. Fauna of Saudi Arabia, 9, 169–450. Grossmann, W., Kowalski, T., Zwanzig, B. M., & Zilger, H. J. (2012): Ergänzende herpetologi-

sche Beobachtungen auf dem Saiq-Plateau und im Jebel al-Akhdar, Sultanat Oman. Sauria, 34(4), 3–18.

Dow

nloa

ded

by [

81.6

1.17

4.21

6] a

t 14:

20 2

7 Ju

ne 2

016

8 P. de Pous et al.

Guindon, S., & Gascuel, O. (2003): A simple, fast, and accurate algorithm to estimate large phy-logenies by maximum likelihood. Systematic Biology, 52, 696–704.

Huelsenbeck, J. P., & Rannala, B. (2004): Frequentist properties of Bayesian posterior probabili-ties of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53, 904–913.

Katoh, K., & Standley, D. M. (2013): MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.

Lambeck, K. (1996): Shoreline reconstructions for the Persian Gulf since the last glacial maxi-mum. Earth and Planetary Science Letters, 142, 43–57.

Lenk, P., Kalyabina, S., Wink, M., & Joger, U. (2001): Evolutionary relationships among the true vipers (Reptilia: Viperidae) inferred from mitochondrial DNA sequences. Molecular Phylo-genetics and Evolution, 19, 94–104.

Leviton, A. E., Anderson, S. C., Adler, K., & Minton, S. A. (1992): Handbook to Middle East Amphibians and Reptiles. Oxford (Ohio): Society for the Study of Amphibians and Reptiles.

Metallinou, M., Cervenka, J., Crochet, P. A., Kratochvíl, L., Wilms, T., Geniez, P., Shobrak, M. Y., Brito, J. C., & Carranza, S. (2015): Species on the rocks: Systematics and biogeography of the rock-dwelling Ptyodactylus geckos (Squamata: Phyllodactylidae) in North Africa and Arabia. Molecular Phylogenetics and Evolution 85, 208–220.

Papenfuss, T. J., Jackman, T., Bauer, A., Stuart, B. L., Robinson, M. D., & Parham, J. F. (2009): Phylogenetic relationships among species in the Sphaerodactylid lizard genus Pristurus. Pro-ceedings of the California Academy of Sciences, 60, 675.

Pyron, R. A., Burbrink, F. T., & Wiens, J. J. (2013): A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93.

Rambaut, A., & Drummond, A. J. (2009): Tracer v1. 5. http://tree.bio.ed.ac.uk/software/tracer [accessed on December 2015].

Sindaco, R., Venchi, A., Grieco, C. (2013): The reptiles of the Western Palearctic. Volume 2: Annotated checklist and distributional atlas of the snakes of Europe, North Africa, Middle East and Central Asia, with an Update to Volume 1. Latine: Societas Herpetologica Italica.

Šmíd, J., Carranza, S., Kratochvíl, L., Gvoždík, V., Nasher, A. K., & Moravec, J. (2013): Out of Arabia: A complex biogeographic history of multiple vicariance and dispersal events in the gecko genus Hemidactylus (Reptilia: Gekkonidae). PLoS ONE, 8, e64018.

Stamatakis, A. (2006): RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011): MEGA5: mo-lecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

Uetz, P. (2015): The reptile database. www.reptile-database.org [accessed in December 2015]. van der Kooij, J. (2001): The herpetofauna of the Sultanate of Oman. Part 4: The terrestrial

snakes. Podarcis, 2, 54–64. Wilcox, T. P., Zwickl, D. J., Heath, T. A., & Hillis, D. M. (2002): Phylogenetic relationships of

the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic sup-port. Molecular Phylogenetics and Evolution, 25, 361–371.

Xia, X. (2013): DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 30, 1720–1728.

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Supplementary Material to: Phylogeny and biogeography of Arabian populations of the

Persian Horned Viper Pseudocerastes persicus (Duméril, Bibron & Duméril, 1854)

Philip de Pous, Marc Simó-Riudalbas, Johannes Els, Sithum Jayasingh, Felix Amat and Salvador Carranza

Zoology in the Middle East, 62, 2016

http://dx.doi.org/10.1080/09397140.2016.1202896

 

 

Supplementary Figure S1. Detailed altitudinal map of the Jebel Akhdar area showing the distribution of Pseudocerastes persicus and the three new records reported herein. Locality numbers correspond to localities from Fig. 1 and Table 1.

Supplementary Figure S2. A) Photo of the road-killed specimen of Pseudocerastes persicus (specimen CN205 in Table 1) observed on 10 May 2013 in a steep curve while descending the road from Sayq to Birkat Al Mouz (23.00036, 57.70227, 1589 m a.s.l.); B) photo of the live P. persicus (specimen CN675 in Table 1) observed on the 21 May 2013 on Jebel Kawr (23.14561 N, 57.03327 E, 2270 m a.s.l.); C) Photo of the live P. persicus (specimen CN886 in Table 1) observed on 22 May 2013 close to Jebel Shams, about 5 km west of the village of Karb (23.2814 N, 57.16291 E, 2116 m a.s.l); D) Photo of the live P. persicus (specimen CN10306 in Table 1) observed on 17 October 2015 on the Hajar mountain range along the east coast of Sharjah, UAE (25.03839 N, 56.21765 E, 815 m a.s.l.).

 

Supplementary Table S1. Detailed information on the specimens used in the phyloge-netic analyses. Voucher codes of specimens available in collections refer to the follow-ing collections: HLMD: Hessisches Landesmuseum, Darmstadt; IBE: Institute of Evolu-tionary Biology (CSIC-UPF), Barcelona, Spain. The asterisk (*) indicates that there is no numbered code. Taxon Specimen Voucher code Country Locality GenBank

E. macmahoni Pakistan HM179464 E. macmahoni HLMD RA-2890 Pakistan AJ275711

P. fieldi Collection Michael Lehmann* Israel AJ275716

P. persicus HLMD RA-1724 Pakistan AJ275717 P. persicus 25 Iran Damghan KF314705 P. persicus 27 Iran Maybod KF314706 P. persicus 30 Iran Ilam KF314707 P. persicus 30k Iran Ilam KF314708 P. persicus 32 Iran Ilam KF314709 P. persicus 1000 Iran Ilam KF314710 P. persicus 20 Iran Bazman KF314711 P. persicus 21 Iran Bandar-e-Abbas KF314712 P. persicus 22 Iran Saraj KF314713 P. persicus CN675 IBE CN675 Oman Jebel Kawr (2) KX343210 P. persicus CN205 Oman Sayq plateau (1) KX343211 P. persicus CN886 IBE CN886 Oman Jebel Shams (3) KX343212 P. persicus CN10306 UAE Sharjah (4) KX343213 P. urarachnoides 24 Iran Ilam KF314714 P. urarachnoides 31k Iran Ilam KF314715 P. urarachnoides 1064 Iran Ilam KF314716 P. urarachnoides Iran Ilam KF314717

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