Abstract
Mesalina are small diurnal lacertid lizards inhabiting arid areas from North Africa to northwestern India. Previous phylogenetic studies have shown the existence of several species complexes within the genus, some of them with high levels of undiscovered diversity. In the present study, we carry out an integrative systematic revision of the Mesalina guttulata species complex using both molecular and morphological data from across its entire distribution range in North Africa, the Middle East and Arabia. The results of the genetic analyses indicate that M. guttulata and M. bahaeldini are two allopatric sister taxa separated by the Suez Canal and that the species complex includes a further three unnamed deep phylogenetic lineages, two of them restricted to southern and southwestern Arabia and described herein as Mesalina austroarabica sp. nov. and Mesalina arnoldi sp. nov., respectively. As a result of the lack of enough material, the third deep lineage, distributed across Kuwait, Saudi Arabia and Jordan, is provisionally left undescribed. The two newly described species are characterized by their size, scale counts and tail coloration, as well as differences at the three mitochondrial and one nuclear gene analyzed in the present study.
References
Anderson, S.C. (1999) The lizards of Iran. Society for the Study of Amphibians and Reptiles, Oxford and Ohio, 442 pp.
Arnold, E.N. (1980) The scientific results of the Oman flora and fauna survey 1977 (Dhofar). The Reptiles and Amphibians of Dhofar, southern Arabia. Journal of Oman studies special seport, 2, 273–332.
Arnold, E.N. (1986a) A key and annotated checklist to the lizards and amphisbaenians of Arabia. Fauna of Saudi Arabia, 8, 385–435.
Arnold, E.N. (1986b) The hemipenis of lacertid lizards (Reptilia: Lacertidae): structure, variation and systematic implications. Journal of Natural History, 20 (5), 1221–1257.
https://doi.org/10.1080/00222938600770811Arnold, E.N. (1986c) Why copulatory organs provide so many useful taxonomic characters: the origin and maintenance of hemipenial differences in lacertid lizards (Reptilia: Lacertidae). Biological Journal of the Linnean Society, 29 (4), 263–281.
https://doi.org/10.1111/j.1095-8312.1986.tb00279.xArnold, E.N., Arribas, O. & Carranza, S. (2007) Systematics of the Palaearctic and Oriental lizard tribe Lacertini (Squamata : Lacertidae : Lacertinae), with descriptions of eight new genera. Zootaxa, 1430 (1), 1–86.
https://doi.org/10.11646/zootaxa.1430.1.1Arnold, E.N., Robinson, M.D. & Carranza, S. (2009) A preliminary analysis of phylogenetic relationships and biogeography of the dangerously venomous carpet vipers, Echis (Squamata, Serpentes, Viperidae) based on mitochondrial DNA sequences. Amphibia-Reptilia, 30 (2), 273–282.
https://doi.org/10.1163/156853809788201090Badiane, A., Garcia-Porta, J., Červenka, J., Kratochvíl, L., Sindaco, R., Robinson, M.D., Morales, H., Mazuch, T., Price, T. & Amat, F. (2014) Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris. Zootaxa, 3835 (1), 33–58.
https://doi.org/10.11646/zootaxa.3835.1.2Baha El Din, S. (2006) A Guide to the Reptiles and Amphibians of Egypt. The American University in Cairo Press, Cairo and New York, 359 pp.
Boulenger, G.A. (1921) Monograph of the Lacertidae. Vol. II. British Museum (Natural History), London, 451 pp.
Carranza, S. & Arnold, E.N. (2012) A review of the gecko genus Hemidactylus (Squamata: Gekkonidae) from Oman based on morphology, mitochodrial and nuclear data, with descriptions of eight new species. Zootaxa, 3378, 1–95.
Carranza, S., Simó-Riudalbas, M., Jayasinghe, S., Wilms, T. & Els, J. (2016) Microendemicity in the northern Hajar Mountains of Oman and the United Arab Emirates with the description of two new species of geckos of the genus Asaccus (Squamata: Phyllodactylidae). PeerJ, 4, e2371.
https://doi.org/10.7717/peerj.2371Carranza, S., Xipell, M., Tarroso, P., Gardner, A., Arnold, E.N., Robinson, M.D., Simó-Riudalbas, M., Vasconcelos, R., de Pous, P., Amat, F., Šmíd, J., Sindaco, R., Metallinou, M., Els, J., Pleguezuelos, J.M., Machado, L., Donaire, D., Martínez, G., Garcia-Porta, J., Mazuch, T., Wilms, T., Gebhart, J., Aznar, J., Gallego, J., Zwanzig, B.M., Fernández-Guiberteau, D., Papenfuss, T., Al Saadi, S., Alghafri, A., Khalifa, S., Al Farqani, H., Bilal, S.B., Alzari, I.S., Al Adhoobi, A.S., Al Omairi, Z.S., Al Shariani, M., Al Kiyumi, A., Al Sariri, T., Al Shukaili, A.S., Al Akhzami, S.N. (2018) Diversity, distribution and conservation of the terrestrial reptiles of Oman (Sauropsida, Squamata). PLoS ONE, 13 (2), e0190389.
https://doi.org/10.1371/journal.pone.0190389Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.
https://doi.org/10.1046/j.1365-294x.2000.01020.xDrummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29 (8), 1969–1973.
https://doi.org/10.1093/molbev/mss075Felsenstein, J. (1985) Confidence-limits on phylogenies: an approach using the bootstrap. Evolution, 39 (4), 783–791.
https://doi.org/10.1111/j.1558-5646.1985.tb00420.xFlot, J.F. (2010) seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources, 10 (1), 162–166.
https://doi.org/10.1111/j.1755-0998.2009.02732.xGarcia-Porta, J., Simó-Riudalbas, M., Robinson, M. & Carranza, S. (2017) Diversification in arid mountains: biogeography and cryptic diversity of Pristurus rupestris rupestris in Arabia. Journal of Biogeography, 44 (8), 1694–1704.
https://doi.org/10.1111/jbi.12929Gardner, A.S. (2013) The amphibians and reptiles of Oman and the UAE. Edition Chimaira, Frankfurt am Main, 480 pp.
Harrigan, R.J., Mazza, M.E. & Sorenson, M.D. (2008) Computation vs. cloning: evaluation of two methods for haplotype determination. Molecular Ecology Resources, 8 (6), 1239–1248.
https://doi.org/10.1111/j.1755-0998.2008.02241.xHuelsenbeck, J.P. & Rannala, B. (2004) Frequentist Properties of Bayesian Posterior Probabilities of Phylogenetic Trees Under Simple and Complex Substitution Models. Systematic Biology, 53 (6), 904–913.
https://doi.org/10.1080/10635150490522629Joger, U. & Mayer, W. (2002) A new species of Mesalina (Reptilia:Lacertidae) from Abd al-Kuri, Socotra Archipelago, Yemen, and a preliminary molecular phylogeny for the genus Mesalina. Fauna of Arabia, 19, 497–505.
Kapli, P., Lymberakis, P., Crochet, P., Geniez, P., Brito, J.C., Almutairi, M., Ahmadzadeh, F., Schmitz, A., Wilms, T. & Pouyani, N.R. (2015) Historical biogeography of the lacertid lizard Mesalina in North Africa and the Middle East. Journal of Biogeography, 42 (2), 267–279.
https://doi.org/10.1111/jbi.12420Kapli, P., Lymberakis, P., Poulakakis, N., Mantziou, G., Parmakelis, A. & Mylonas, M. (2008) Molecular phylogeny of three Mesalina (Reptilia: Lacertidae) species (M. guttulata, M. brevirostris and M. bahaeldini) from North Africa and the Middle East: Another case of paraphyly? Molecular Phylogenetics and Evolution, 49 (1), 102–110.
https://doi.org/10.1016/j.ympev.2008.06.016Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.
https://doi.org/10.1093/molbev/mst010Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., Drummond, A.J. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199van der Kooij, J. (2001) The herpetofauna of the Sultanate of Oman. Part 3: the true lizards, skinks and monitor lizard. Podarcis, 2 (1), 15–26.
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29 (6), 1695–1701.
https://doi.org/10.1093/molbev/mss020Lichtenstein, H.M.C. (1823) Verzeichnifs der Doubletten des zoologischen Museums der Königl. Universität zu Berlin nebst Beschreibung vieler bisher unbekannter Arten von Säugethieren, Vögeln, Amphibien und Fischen. In Commission bei T. Trautwein, Berlin, 118 pp.
Machado, L., Šmíd, J., Mazuch, T., Sindaco, R., Al Shukaili, A.S. & Carranza, S. (2018) Systematics of the Saharo-Arabian clade of the Palearctic naked-toed geckos with the description of a new species of Tropiocolotes endemic to Oman. Journal of Zoological Systematics and Evolutionary Research. [in press]
Mayer, W. & Pavlicev, M. (2007) The phylogeny of the family Lacertidae (Reptilia) based on nuclear DNA sequences: convergent adaptations to arid habitats within the subfamily Eremiainae. Molecular Phylogenetics and Evolution, 44 (3), 1155–1163.
https://doi.org/10.1016/j.ympev.2007.05.015Metallinou, M. & Carranza, S. (2013) New species of Stenodactylus (Squamata: Gekkonidae) from the Sharqiyah Sands in northeastern Oman. Zootaxa, 3745 (4), 449–468.
https://doi.org/10.11646/zootaxa.3745.4.3Metallinou, M., Červenka, 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.
https://doi.org/10.1016/j.ympev.2015.02.010Moravec, J. (2004) Distribution and morphological variation of the lizard Mesalina brevirostris in Syria. In: Pérez-Mellado, V., Riera, N & Perera, A. (Eds.), The biology of lacertid lizards. Evolutionary and ecological perspectives. Institut Menorquí d’Estudis, Menorca, pp. 245–257.
de Pous, P., Machado, L., Metallinou, M., Červenka, J., Kratochvíl, L., Paschou, N., Mazuch, T., Šmíd, J., Simó-Riudalbas, M., Sanuy, D. & Carranza, S. (2016) Taxonomy and biogeography of Bunopus spatalurus (Reptilia; Gekkonidae) from the Arabian Peninsula. Journal of Zoological Systematics and Evolutionary Research, 54 (1), 67–81.
https://doi.org/10.1111/jzs.12107
R Development Core Team (2016) R: a language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org/ (accessed 11 April 2016)
Rambaut, A. & Drummond, A.J. (2013) Tracer v1.5. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 1 May 2018)
Schätti, B. & Desvoignes, A. (1999) The herpetofauna of Southern Yemen and the Sokotra Archipelago. Instrumenta Biodiversitatis IV, Muséum d'Histoire Naturelle, Genève, 178 pp.
Schätti, B. & Gasperetti, J. (1994) A contribution to the herpetofauna of Southwest Arabia. Fauna of Saudi Arabia, 14, 348–423.
Segoli, M., Cohen, T., & Werner, Y.L. (2002) A new lizard of the genus Mesalina from Mt. Sinai, Egypt. Faunistiche Abhandlungen Staatliches Museum für Tierkunde Dresden, 23 (9), 157–176.
Silvestro, D. & Michalak, I. (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, 12 (4), 335–337.
https://doi.org/10.1007/s13127-011-0056-0Simó-Riudalbas, M., Metallinou, M., de Pous, P., Els, J., Jayasinghe, S., Péntek-Zakar, E., Wilms, T., Al-Saadi, S. & Carranza, S. (2017) Cryptic diversity in Ptyodactylus (Reptilia: Gekkonidae) from the northern Hajar Mountains of Oman and the United Arab Emirates uncovered by an integrative taxonomic approach. PLoS ONE, 12 (8), e0180397.
https://doi.org/10.1371/journal.pone.0180397Simó-Riudalbas M., Tarroso P., Papenfuss T., Al-Sariri T., & Carranza S. (2018) Systematics, biogeography and evolution of Asaccus gallagheri (Squamata, Phyllodactylidae) with the description of a new endemic species from Oman. Systematics and Biodiversity, 16 (4), 323–339.
https://doi.org/10.1080/14772000.2017.1403496
Sindaco, R. & Jeremcenko, V.K. (2008) The reptiles of the Western Palearctic. Annotated checklist and distributional atlas of the turtles, crocodiles, amphisbaenians and lizards of Europe, North Africa, Middle East and Central Asia. Monografie della Societas Herpetologica Italica, I, 1–579.
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 (5), e64018.
https://doi.org/10.1371/journal.pone.0064018Šmíd, J. & Frynta, D. (2012) Genetic variability of Mesalina watsonana (Reptilia: Lacertidae) on the Iranian plateau and its phylogenetic and biogeographic affinities as inferred from mtDNA sequences. Acta Herpetologica, 7 (1), 139–153.
http://doi.org/10.13128/Acta_Herpetol-10193Šmíd, J., Moravec, J., Gvoždík, V., Štundl, J., Frynta, D., Lymberakis, P., Kapli, P., Wilms, T., Schmitz, A. & Shobrak, M. (2017a) Cutting the Gordian Knot: Phylogenetic and ecological diversification of the Mesalina brevirostris species complex (Squamata, Lacertidae). Zoologica Scripta, 46 (6), 649–664.
https://doi.org/10.1111/zsc.12254Šmíd, J., Moravec, J., Kratochvíl, L., Nasher, A.K., Mazuch, T., Gvoždík, V. & Carranza, S. (2015) Multilocus phylogeny and taxonomic revision of the Hemidactylus robustus species group (Reptilia, Gekkonidae) with descriptions of three new species from Yemen and Ethiopia. Systematics and Biodiversity, 13 (4), 346–368.
https://doi.org/10.1080/14772000.2014.996264Šmíd, J., Shobrak, M., Wilms, T., Joger, U. & Carranza, S. (2017b) Endemic diversification in the mountains: genetic, morphological and geographical differentiation of the Hemidactylus geckos in southwestern Arabia. Organisms Diversity and Evolution, 17 (1), 267–285.
https://doi.org/10.1007/s13127-016-0293-3Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.
https://doi.org/10.1093/bioinformatics/btl446Stresemann, E. (1954) Hemprich und Ehrenberg Reisen zweier naturforschender Freunde im Orient, geschildert in ihren Briefen aus den Jahren 1819-1826. Abhandlungen der Deutschen Akademie Wissenschaften zu Berlin. Klasse fur Mathematik und Allgemeine Naturwissenschaften, 1954 (1), 1–177.
Szczerbak, N. (1974) Yaschurki Palearktiki. Akademiya Nauk Ukrainskoi SSR Institut Zoologii, Naukova Dumka, Kiev, 296 pp.
Szczerbak, N. (1989) Catalogue of the African Sand Lizards (Reptilia: Sauria: Eremiainae: Lampieremias, Pseuderemias, Taenieremias, Mesalina, Meroles). Herpetozoa, 1 (3/4), 119–132.
Tamar, K., Carranza, S., Sindaco, R., Moravec, J., Trape, J.F. & Meiri, S. (2016) Out of Africa: phylogeny and biogeography of the widespread genus Acanthodactylus (Reptilia: Lacertidae). Molecular Phylogenetics and Evolution, 103, 6–18.
https://doi.org/10.1016/j.ympev.2016.07.003Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.
https://doi.org/10.1093/molbev/mst197Uetz, P., Goll, J. & Hallerman, J. (2017) The reptile database. Available from http://www.reptile-database.org (accessed 3 February 2017)
Vasconcelos, R. & Carranza, S. (2014) Systematics and biogeography of Hemidactylus homoeolepis Blanford, 1881 (Squamata: Gekkonidae), with the description of a new species from Arabia. Zootaxa, 3835 (4), 501–527.
https://doi.org/10.11646/zootaxa.3835.4.4Werner, Y.L. & Ashkenazi, S. (2010) Notes on some Egyptian Lacertidae, including a new subspecies of Mesalina, involving the Seligmann effect. Turkish Journal of Zoology, 34, 123–133.
https://doi.org/10.3906/zoo-0905-8Wilcox, 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 support. Molecular Phylogenetics and Evolution, 25 (2), 361–371.
https://doi.org/10.1016/S1055-7903(02)00244-0