Abstract
Based on newly provided morphological and previously published genetic data, we describe two new distinctive sympatric lacertid lizards of the genus Eremias (subgenus Aspidorhinus) from the arid mountains of northwestern Balochistan Province, Pakistan. The new species, Eremias killasaifullahi sp. nov. and Eremias rafiqi sp. nov. are distinguished from all other species of the subgenus Aspidorhinus (E. afghanistanica, E. fahimii, E. isfahanica, E. kopetdaghica, E. lalezharica, E. montana, E. nikolskii, E. papenfussi, E. persica, E. regeli, E. roborowskii, E. strauchi, E. suphani, and E. velox) by unique morphological characters and genetic differentiation. In the molecular phylogeny of Aspidorhinus, both new taxa are well-supported lineages differentiated from other species of this subgenus by uncorrected p distances from 8.5% to 21.6%, respectively. Both new species belong to E. persica complex where E. rafiqi sp. nov. is partly similar in dorsal color pattern to E. persica but can be distinguished from this species by unique meristic and morphometric characters. Eremias rafiqi sp. nov. is found in Pakistan, Afghanistan, and eastern Iran. Eremias killasaifullahi sp. nov. can be differentiated from E. persica by its distant distribution, dorsal color and pattern, smaller size, and less number of gulars and ventral scales. Eremias killasaifullahi sp. nov. is only known from the type locality and represents the local microendemism, along with other endemic species of reptiles reported from this part of Pakistan. We, however, expect that E. killasaifullahi sp. nov. could have a broader range in northwestern Pakistan and southeastern Afghanistan, which should be an object of following investigations. Our data show that remote areas between Hindu Kush Mountains and Indus River need attention as they most probably represent possible sources of genetic and species diversity in the region.
References
Agarwal, I. & Ramakrishnan, U. (2017) A phylogeny of open-habitat lizards (Squamata: Lacertidae: Ophisops) supports the antiquity of Indian grassy biomes. Journal of Biogeography, 44, 2021–2032. https://doi.org/10.1111/jbi.12999
Agarwal, I., Khandekar, A., Ramakrishnan, U., Vyas, R. & Giri, V.B. (2017) Two new species of the Ophisops microlepis (Squamata: Lacertidae) complex from northwestern India with a key to Indian Ophisops. Journal of Natural History, 52, 819–847. https://doi.org/10.1080/00222933.2018.1436203
Alcock, A.W. & Finn, F. (1896) An account of the Reptilia collected by Dr. F.P. Maynard, Captain A.H. McMahon, C.I.E., and the members of the Afghan-Baluch Boundary Commission of 1896. The journal of the Asiatic Society of Bengal, 65, 550–566.
Ananjeva, N., Borkin, L.Y., Darevsky, I. & Orlov, N. (1998) Encyclopedia of Russian Nature. Amphibians and Reptiles. ABF, Moscow, 574 pp.
Anderson, S.C. & Leviton, A.E. (1967) A new species of Eremias (Reptilia: Lacertidae) from Afghanistan. Occasional Papers of the California Academy of Sciences, 64, 1–4.
Anderson, S.C. (1999) The Lizards of Iran. Society for the Study of Amphibians and Reptiles, Oxford, Ohio, 442 pp.
Arnold, E.N. (1986) The hemipenis of lacertid lizards (Reptilia: Lacertidae): structure, variation and systematic implications. Journal of Natural History, 20, 1221–1257. https://doi.org/10.1080/00222938600770811
Arnold, E.N. (1989) Towards a phylogeny and biogeography of the Lacertidae: relationships within an Old-World family of lizards derived from morphology. Bulletin of the British Museum (Natural History), 55, 209–257.
Baig, K.J. & Masroor, R. (2006) A new species of Eremias (Sauria: Lacertidae) from Cholistan Desert, Pakistan. Russian Journal of Herpetology, 13, 167–174.
Baig, K.J. (1998) A new species of Tenuidactylus (Sauria: Gekkonidae) from Balochistan, Pakistan. Hamadryad, 23, 127–132.
Baig, K.J. (1999) Description and ecology of a new subspecies of Black Rock Agama, Laudakia melanura (Sauria: Agamidae) from Balochistan, Pakistan. Russian Journal of Herpetology, 6, 81–86.
Barabanov, A.V. (2009) Aspidorhinus Eichwald, 1841 as a valid subgeneric name for Eremias velox species group (Sauria, Lacertidae). Current Studies in Herpetology, 9, 59–61. [in Russian, with English summary]
Başoğlu, M. & Hellmich, W. (1968) Eine neue Eremias-Form aus Ost-Anatolien (Reptilia, Lacertidae). Ege Üniversitesi Fen Fakültesi Ýlmi Raporlar Serisi, Bornova-Ýzmir, 67, 3–7.
Bedriaga, J. von (1912) Wissenschaftliche Resultate der von N. M. Przewalski nach Central-Asien unternommenen Reisen, Zoologischer Theil. Band III, Abtheilung 1. Amphibien und Reptilien. Kaiserliche Akademie der Wissenschaften, St. Petersburg, 769 pp. [in Russian and German]
Bedriaga, J.V. (1905) Neue Saurier aus Russisch-Asien. Annu. In: Nikolsky, A.M. (Ed.), Herpetologia rossica. Mémoires de l`Académie impériale des sciences de St. Pétersbourg, XVII (1), pp. 1–518.
Bischoff, W. & Böhme, W. (1980) Der systematische Status der türkischen Wüstenrenner des Subgenus Eremias (Sauria: Lacertidae). Zoologische Beiträge, 26, 297–306.
Blanford, W.T. (1875) List of Reptilia and Amphibia collected by the late Dr. Stoliczka in Kashmir, Ladák, eastern Turkestán, and Wakhán, with descriptions of new species. The journal of the Asiatic Society of Bengal, 44 (Pt. 2, No. 3), 191–196.
Böhme, W. & Sczczerbak, N.N. (1991) Ein neuer Wüstenrenner aus dem Hochland Afghanistans, Eremias (Eremias) afghanistanica sp. n. (Reptilia: Sauria: Lacertidae). Bonner zoologische Beiträge, 42, 137–141.
Boulenger, G.A. (1890) The Fauna of British India, Including Ceylon and Burma. Reptilia and Batrachia. Secretary of State for India in Council, Taylor & Francis Printers, London, 541 pp.
Boulenger, G.A. (1918) A synopsis of the lizards of the genus Eremias. Journal of Zoological Research, 3, 1–12.
Boulenger, G.A. (1921) Monograph of the Lacertidae. Vol. 2. British Museum (Natural History), Cromwell Road, London, 451 pp. https://doi.org/10.5962/bhl.title.54022
Chirikova, M.A. (2004) Variability of Eremias velox Pallas, 1771 (Reptilia, Sauria) from Kazakhstan. Selivia, 2004, 24–34. [in Russian]
Clark, R.J., Clark, E.D., Anderson, S.C. & Leviton, A.E. (1969) Report on a collection of amphibians and reptiles from Afghanistan. Proceedings of the California Academy of Sciences, Series 4, 36, 279–316.
Clement, 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.x
Darevsky, I.S. & Shcherbak, N.N. (1978) Eremias andersoni, a new lizard (Reptilia, Lacertilia, Lacertidae) from Iran. Journal of Herpetology, 12, 13–15. https://doi.org/10.2307/1563496
Flot, J.F. (2010) SeqPhase: a web tool for interconverting phase input/output files and fasta sequence alignments. Molecular Ecology Resources, 10, 162–166. https://doi.org/10.1111/j.1755-0998.2009.02732.x
Fraser, D.J. & Bernatchez, L. (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology, 10, 2741–2752. https://doi.org/10.1046/j.1365-294X.2001.t01-1-01411.x
Gholamifard, A. & Rastegar-Pouyani, N. (2015) First record and range extension of Sistan racerunner, Eremias fasciata, Blanford 1874, (Sauria: Lacertidae) from Hormozgan Province, southern Iran. Amphibian and Reptile Conservation, 9, 54–57.
Guo, X.G., Chen, D.L., Papenfuss, T.J., Ananjeva, N.B., Melnikov, D.A. & Wang, Y. (2011) Phylogeny and divergence times of some racerunner lizards (Lacertidae: Eremias) inferred from mitochondrial 16S rRNA gene segments. Molecular Phylogenetics and Evolution, 61, 400–412. https://doi.org/10.1016/j.ympev.2011.06.022
Guo, X.G., Chen, D.L., Wan, H.F. & Wang, Y.Z. (2010) Review of systematics of the racerunner lizard (Lacertidae: Eremias). Sichuan Journal of Zoology, 29, 665–672. [in Chinese with English abstract]
Jablonski, D. & Masroor, R. (2021) First record of Eremias kakari Masroor et al., 2020 (Squamata: Lacertidae) for Afghanistan. Bonn Zoological Bulletin, 70, 63–65. https://doi.org/10.20363/BZB-2021.70.1.063
Jablonski, D., Basit, A., Farooqi, J., Masroor, R. & Böhme, W. (2021) Biodiversity research in a changing Afghanistan. Science, 372 (6549), 1402. https://doi.org/10.1126/science.abj8118
Kessler, K.F. (1878) Transcaucasian voyage. Travaux de la Société des Naturalistes de St. Pétersbourg, 8 (Supplement), 1–200. [in Russian]
Khan, M.A., Jablonski, D., Nadeem, M.S., Masroor, R., Kehlmaier, C., Spitzweg, C. & Fritz, U. (2021) Molecular phylogeny of Eremias spp. from Pakistan contributes to a better understanding of the diversity of racerunners. Journal of Zoological Systematics and Evolutionary Research, 59, 466–483. https://doi.org/10.1111/jzs.12426
Khan, M. S. (2006) Amphibians and reptiles of Pakistan. Krieger Publishing Company, Malabar, Florida, 311 pp.
Khan, M.S. & Ahmed, N. (1987) On a collection of amphibians and reptiles from Baluchistan, Pakistan. Pakistan Journal of Zoology, 19, 361–370.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773. https://doi.org/10.1093/molbev/msw260
Lantz, L.A. (1928) Les Eremias de l’Asie Occidentale. Bulletin du Museum de Géorgie, 4, 1–136.
Masroor, R. (2012) A contribution to the herpetology of northern Pakistan: The amphibians and reptiles of Margalla Hills National Park and surrounding regions. Society for the Study of Amphibians and Reptiles (SSAR), Ithaca, New York and Chimaira Buchhandelsgesellschaft mbH, Edition, 217 pp.
Masroor, R., Khisroon, M., Khan, M.A. & Jablonski, D. (2020a) A new species of Microgecko Nikolsky, 1907 (Squamata: Gekkonidae) from Pakistan. Zootaxa, 4780 (1), 147–164. https://doi.org/10.11646/zootaxa.4780.1.7
Masroor, R., Khisroon, M., Khan, M.A. & Jablonski, D. (2020b) A new species of Eremias Fitzinger, 1834 (Squamata: Lacertidae) from the arid mountains of Pakistan. Zootaxa, 4786 (1), 101–121. https://doi.org/10.11646/zootaxa.4786.1.8
Mertens, R. (1969) Die Amphibien und Reptilien West-Pakistans. Stuttgarter Beiträge zur Naturkunde, 197, 1–96.
Minton, S.A. (1966) A contribution to the herpetology of West Pakistan. Bulletin of the American Museum of Natural History, 134, 28–184.
Moravec, J. (1994) A new lizard from Iran, Eremias (Eremias) lalezharica sp. n. (Reptilia: Lacertilia: Lacertidae). Bonner zoologische Beiträge, Bonn, 45, 61–66.
Mozaffari, O., Ahmadzadeh, F. & Parham, J.F. (2011) Eremias papenfussi sp. nov., a new lacertid lizard (Sauria: Lacertidae) from Tehran Province, Iran. Zootaxa, 3114 (1), 57–62. https://doi.org/10.11646/zootaxa.3114.1.6
Mozaffari, O., Ahmadzadeh, F. & Saberi-Pirooz, R. (2020) Fahimi’s racerunner, a new species of the genus Eremias Fitzinger, 1834 (Sauria: Lacertidae) from Iran. Zootaxa, 4768 (4), 565–578. https://doi.org/10.11646/zootaxa.4768.4.7
Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300.
Nikolsky, A.M. (1896) Diagnoses reptilium et amphibiorum novorum in Persia orientali a N. Zarudny collectorum. Annuaire Musée Zoologique de l’Académie Impériale des Sciences de St.-Pétersbourg, 1, 369–372.
Nikolsky, A.M. (1905) Herpetologia rossica. Mémoires Académie Impériale des Sciences, Physics-Math. Classe, St. Pétersbourg, 17, 1–518.
Nikolsky, A.M. (1915) Faune de la Russie, Reptiles Vol. 1 Chelonia et Sauria. Reptiles of Russia and adjacent countries. Reptiles (Reptilia). Vol. 1. Imperial Saint Petersburg Academy of Sciences, Saint Petersburg, 532 pp. [in Russian, translated from Russian by the Israel Program for Scientific Translations 1963]
Orlova, V.F., Poyarkov, N.A., Chirikova, M.A., Nazarov, R.A., Munkhbataar, M., Munkhbayar, K. & Terbish, K. (2017) MtDNA differentiation and taxonomy of Central Asian racerunners of Eremias multiocellata-E. przewalskii species complex (Squamata, Lacertidae). Zootaxa, 4282 (1), 1–42. https://doi.org/10.11646/zootaxa.4282.1.1
Pyron, R., Burbrink, F. & Wiens, J. (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93. https://doi.org/10.1186/1471-2148-13-93
Rastegar-Pouyani, E., Hosseinian Yousefkhani, S.S. & Wink, M. (2015) Taxonomic reevaluation of Eremias strauchi strauchi Kessler, 1878 and Eremias strauchi kopetdaghica Szczerbak, 1972, based on nuclear and mitochondrial DNA sequences (Reptilia: Lacertidae). Zoology in the Middle East, 61, 118–124. https://doi.org/10.1080/09397140.2015.1020615
Rastegar-Pouyani, E., Noureini, S.K., Rastegar-Pouyani, N., Joger, U. & Wink, M. (2012) Molecular phylogeny and intraspecific differentiation of the Eremias velox complex of the Iranian Plateau and Central Asia (Sauria, Lacertidae). Journal of Zoological Systematics and Evolutionary Resresearch, 50, 220–229. https://doi.org/10.1111/j.1439-0469.2012.00662.x
Rastegar-Pouyani, E., Rastegar-Pouyani, N., Kazemi-Noureini, S., Joger, U. & Wink, M. (2010) Molecular phylogeny of the Eremias persica complex of the Iranian plateau (Reptilia: Lacertidae), based on mtDNA sequences. Zoological Journal of the Linnaean Society, 158, 641–660. https://doi.org/10.1111/j.1096-3642.2009.00553.x
Rastegar-Pouyani, E., Yousefkhani Hosseinian, S.S., Soolmaz, R., Kami, H.G., Mehdi, R. & Wink, M. (2016) A new species of the genus Eremias Fitzinger, 1834 (Squamata: Lacertidae) from Central Iran, supported by mtDNA sequences and morphology. Zootaxa, 4132 (2), 207–220. https://doi.org/10.11646/zootaxa.4132.2.2
Rastegar-Pouyani, N. & Nilson, G. (1997) A new species of Eremias (Sauria: Lacertidae) from Fars Province, South-Central Iran. Russian Journal of Herpetology, 4, 94–101. https://doi.org/10.30906/1026-2296-1997-4-2-94-101
Rastegar-Pouyani, N. & Rastegar-Pouyani, E. (2001) A new species of Eremias (Sauria: Lacertidae) from highlands of Kermanshah Province, western Iran. Asiatic Herpetological Research, 9, 107–112. https://doi.org/10.5962/bhl.part.15563
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E. & Sánchez-Gracia, A. (2017) dnasp 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34, 3299–3302. https://doi.org/10.1093/molbev/msx248
Sindaco, R. & Jeremcenko, V.K. (2008) The Reptiles of the Western Palearctic. 1. Annotated Checklist and Distributional Atlas of the Turtles, Crocodiles, Amphisbaenians and Lizards of Europe, North Africa, Middle East and Central Asia. Edizioni Belvedere, Latina, 579 pp.
Šmíd, J., Moravec, J., Kodym, P., Kratochvíl, L., Hosseinian Yousefkhani, S.S. & Frynta. D. (2014) Annotated checklist and distribution of the lizards of Iran. Zootaxa, 3855 (1), 1–97. https://doi.org/10.11646/zootaxa.3855.1.1
Smith, M.A. (1935) The fauna of British India, including Ceylon and Burma. Reptilia and Sauria. Volume II-Sauria. Taylor & Francis, London, 440 pp.
Stephens, M., Smith, N.J. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978–989. https://doi.org/10.1086/319501
Strauch, A.A. (1876) Reptiles and amphibians. In: Przewalski, N.M. (Ed.), Mongolia and the land of Tanguts. Three-year journey in eastern mountainous Asia. Vol. 2. Section 2. Imperial Academy of Sciences, St. Petersburg, pp. 1–55. [in Russian]
Szczerbak, N.N. (1971) Taxonomy of the genus Eremias (Sauria, Reptilia) in connection with the focuses of the desert-steppe fauna development in Palearctic. Vestnik Zoologii, 2, 48–55 [in Russian]
Szczerbak, N.N. (1972) New subspecies of Eremias strauchi-Eremias strauchi kopetdaghica ssp. nova (Sauria, Reptilia) from Turkmenia. Vestnik Zoologii, 6, 83–86 [in Russian]
Szczerbak, N.N. (1974) Racerunners of the Palaearctic. Naukova Dumka Press, Kiev, Ukraine, 296 pp. [in Russian]
Szczerbak, N.N. (1981) Eremias velox (Pallas 1771)—Schneller Wüstenrenner. Handbuch der Reptilien und Amphibien Europas. Band 1 Echsen, I, 447–460.
Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maxi-mum likelihood analysis. Nucleic Acids Research, 44, W232–W235. https://doi.org/10.1093/nar/gkw256
Uetz, P., Freed, P. & Hošek, J. (Eds.) (2020) The Reptile Database. Available from: http://www.reptiledatabase.org (ccessed 13 June 2022)
Wagner, P., Bauer, A.M., Leviton, A.E., Wilms, T.M. & Böhme, W. (2016) A Checklist of the amphibians and reptiles of Afghanistan, Exploring herpetodiversity using biodiversity archives. Proceedings of the California Academy of Sciences, 63, 457–565.