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Vicariant Patterns of Fragmentation Among Gekkonid Lizards of The Molecular Phylogenetics and Evolution Vol. 12, No. 3, August, pp. 320–332, 1999 Article ID mpev.1999.0641, available online at http://www.idealibrary.com on Vicariant Patterns of Fragmentation among Gekkonid Lizards of the Genus Teratoscincus Produced by the Indian Collision: A Molecular Phylogenetic Perspective and an Area Cladogram for Central Asia J. Robert Macey,*,1 Yuezhao Wang,† Natalia B. Ananjeva,‡ Allan Larson,* and Theodore J. Papenfuss§ *Department of Biology, Box 1137, Washington University, St. Louis, Missouri 63130; †Chengdu Institute of Biology, Chengdu, Sichuan, China; ‡Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia; and §Museum of Vertebrate Zoology, University of California, Berkeley, California 94720 Received October 21, 1998; revised December 29, 1998 Key Words: Reptilia; Sauria; Gekkota; Gekkonidae; bio- A well-supported phylogenetic hypothesis is pre- geography; Indian collision; mitochondrial DNA; replica- sented for gekkonid lizards of the genus Teratoscincus. tion; phylogenetics; Asia; China; Kazakhstan; Pakistan. Phylogenetic relationships of four of the five species are investigated using 1733 aligned bases of mitochondrial DNA sequence from the genes encoding ND1 (subunit one The gekkonid lizard genus Teratoscincus is endemic of NADH dehydrogenase), tRNAIle, tRNAGln, tRNAMet, ND2, to the desert regions of central and southwest Asia. tRNATrp, tRNAAla, tRNAAsn, tRNACys, tRNATyr, and COI Five species of Teratoscincus are currently recognized (subunit I of cytochrome c oxidase). A single most parsi- (Macey et al., 1997a). Two species, T. bedriagai and T. monious tree depicts T. przewalskii and T. roborowskii as microlepis, are restricted to desert regions south of the a monophyletic group, with T. scincus as their sister taxon Hindu Kush in Iran, Afghanistan, and Pakistan (Fig. and T. microlepis as the sister taxon to the clade contain- 1). Teratoscincus scincus occurs both in the region of ing the first three species. The aligned sequences contain southwest Asia where T. bedriagai and T. microlepis 341 phylogenetically informative characters. Each node is supported by a bootstrap value of 100% and the shortest are found (Anderson, 1993), as well as to the north in suboptimal tree requires 29 additional steps. Allozymic the Central Asian republics of the former USSR (Kaza- variation is presented for proteins encoded by 19 loci but khstan, Kyrgyzistan, Tadjikistan, Turkmenistan, and these data are largely uninformative phylogenetically. Uzbekistan; Szczerbak and Golubev, 1996). The two Teratoscincus species occur on tectonic plates of Gond- remaining species occur in China and Mongolia. Tera- wanan origin that were compressed by the impinging toscincus przewalskii is found in desert regions of the Indian Subcontinent, resulting in massive montane uplift- Taklimakan, Hami Depression, and low-elevation Gobi. ing along plate boundaries. Taxa occurring in China Teratoscincus roborowskii is restricted to the Turpan De- (Tarim Block) form a monophyletic group showing vicari- pression in China, which is the second lowest depression in ant separation from taxa in former Soviet Central Asia the world. These two species do not overlap in distribution and northern Afghanistan (Farah Block); alternative bio- and are geographically separated from the remaining geographic hypotheses are statistically rejected. This vi- three species by the Tien Shan and Pamir (Macey et al., cariant event involved the rise of the Tien Shan-Pamir 1997a). Prior to the taxonomic revision of Macey et al. and is well dated to 10 million years before present. Using (1997a), T. roborowskii was considered conspecific with T. this date for separation of taxa occurring on opposite scincus, suggesting that populations occurring east of the sides of the Tien Shan-Pamir, an evolutionary rate of Tien Shan-Pamir do not form a monophyletic group (see, 0.57% divergence per lineage per million years is calcu- Szczerbak and Golubev, 1996; Zhao and Adler, 1993). lated. This rate is similar to estimates derived from fish, Phylogenetic patterns of fragmentation are investigated bufonid frogs, and agamid lizards for the same region of in taxa occurring on different tectonic plates of Gondwanan D the mitochondrial genome ( 0.65% divergence per lin- origin now separated by mountain uplifting that resulted eage per million years). Evolutionary divergence of the from the Indian collision. We predict that phylogenetic mitochondrial genome has a surprisingly stable rate relationships in Teratoscincus reflect the historical forma- across vertebrates. tion of faunal barriers by the uplift of the Karakorum, ௠ 1999 Academic Press Pamir, Tien Shan, and Hindu Kush mountains (Fig. 1). Data are reported for nuclear-encoded allozymic 1 To whom correspondence should be addressed. Fax: (314) 935-4432. variation representing 19 loci and mitochondrial DNA 320 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. VICARIANT PATTERNS IN ASIAN Teratoscincus LIZARDS 321 FIG. 1. Map of central and southwest Asia illustrating the approximate distribution of Teratoscincus species relative to major mountain belts and basins. Montane regions that separate Teratoscincus species are depicted with stippling. Note that the mountain chain consisting of the Hindu Kush, Karakoram, Himalaya, Pamir, and Tien Shan all connect, causing a dramatic barrier to the distribution of Teratoscincus species. In addition, the Kopet-Dagh is connected to the Hindu Kush by the Badkyz Plateau (not illustrated) causing a barrier between the Central Asian republics of the former USSR (Kazakhstan, Kyrgyzistan, Tadjikistan, Turkmenistan, and Uzbekistan) and Southwest Asia. The Pamir-Tien Shan is particularly noteworthy because it separates T. przewalskii and T. roborowskii from T. scincus. sequences from the genes encoding ND1 (subunit one of Asia south of the Hindu Kush. Gekko gecko serves as an NADH dehydrogenase), tRNAIle, tRNAGln, tRNAMet, outgroup for both data sets. In the allozymic data, an ND2, tRNATrp, tRNAAla, tRNAAsn, tRNACys, tRNATyr, additional gekkonine outgroup, Cyrtodactylus tibeta- and COI (subunit I of cytochrome c oxidase). Both data nus, is used. An eublepharine species, Eublepharus sets include taxa that occur on each side of the Tien turkmenicus, serves as an additional outgroup for the Shan and Pamir (T. scincus to the west, and T. przewal- mitochondrial DNA sequence data. skii and T. roborowskii to the east); the phylogenetic relationships of these taxa are a major focus of this study. Unfortunately, T. bedriagai, known only from MATERIALS AND METHODS extreme eastern Iran and adjacent Afghanistan, is not available for either data set. The sequence data include Specimen Information representatives of the other four Teratoscincus species Museum numbers and localities for voucher speci- (T. microlepis, T. przewalskii, T. roborowskii, and mens from which DNA was extracted and GenBank T. scincus). Allozymic data were not collected for accession numbers are presented below. Acronyms are T. microlepis, which occurs exclusively in southwest CAS for California Academy of Sciences, San Francisco 322 MACEY ET AL. and MVZ for Museum of Vertebrate Zoology, University TABLE 1 of California at Berkeley. The acronym followed by a dash RM represents a field number of the first author The 19 Allozymic Systems Scored and the Five Electrophoretic Conditions within Which for an uncatalogued specimen being deposited at the They Were Resolved Museum of Vertebrate Zoology. The previously reported sequence for T. przewalskii (Macey et al., 1997b) has Electrophoretic been extended by 19 bases to include 6 additional Enzyme Abbreviation E. C. No. conditionsa amino acid positions and a third codon position of the 1. Aconitase hydratase ACOH-1 4.2.1.3 1 ND1 gene; the GenBank accession has been updated 2. Aconitase hydratase ACOH-2 4.2.1.3 1 accordingly. 3. Aspartate amino- Eublepharus turkmenicus: sequence CAS 184771, transferase AAT 2.6.1.1 3 AF114248, Elev. 300 m, 39° 06Ј N 55° 08Ј E, vicinity of 4. Carboxylic ester b Temen Spring, 2.5 km west of Danata (39° 07Ј N 55° 08Ј hydrolase EST-D 3.1.1.– 3 5. Fructose-bisphos- E) on paved Rd. from Danata to the Ashgabad (Ash- phate aldolase FBA 4.1.2.13 4 kabad) to Krasnovodsk Rd., then 5.4 km south on Dirt 6. Glucose-6-phosphate Rd., Krasnovodsk Region, Turkmenistan. Cyrtodacty- isomerase GPI 5.3.1.9 2 lus tibetanus: allozymes CAS 171751–171760, Elev. 7. Glycerol-3-phosphate 3700 m, at base of mountains, approx 3 km WNW dehydrogenase G3PDH 1.1.1.8 1 8. L-Iditol dehydroge- (airline) of the Potala Palace, Lhasa (29° 39Ј N 91° 06Ј nase IDDH 1.1.1.14 4 E), Lhasa Municipality, Xizang (Tibet) Autonomous 9. Isocitrate dehydroge- Region, China. Gekko gecko: allozymes MVZ 215269, nase IDH-1 1.1.1.42 1 215312, 215314, 215356, 215358–215360, sequence 10. Isocitrate dehydroge- nase IDH-2 1.1.1.42 1 MVZ 215314, AF114249, Patong Beach, Kathu District, 11. L-Lactate dehydroge- Phuket Island, Phuket Province, Thailand. Teratoscin- nase LDH-1 1.1.1.27 3 cus microlepis: sequence MVZ-RM10464, AF114250, 12. L-Lactate dehydroge- captive bred from wild-caught specimens probably origi- nase LDH-2 1.1.1.27 3 nating from Pakistan. Teratoscincus scincus: allozymes 13. Malate dehydroge- nase MDH-1 1.1.1.37 1 MVZ 216056–216065, sequence MVZ 216056, 14. Malate dehydroge- AF114251, near Alma-Ata (43° 15Ј N 76° 57Ј E), Alma- nase MDH-2 1.1.1.37 1 Ata Region, Kazakhstan. Teratoscincus przewalskii: 15. Peptidase B PEP-B 3.4.11.4 4 allozymes CAS 171010–171019, sequence CAS 171010, 16. Peptidase D PEP-D 3.4.13.9 5 U71326 (Macey et al., 1997b,c), Elev. 1000 m, 19.5 km 17. Phosphogluconate dehydrogenase PGDH 1.1.1.44 1 east of the Uygur girl-Hami Mellon monument in the 18. Purine-nucleoside center of Hami (42° 48Ј N 93° 27Ј E), also at km 177.9 phosphorylase PNP 2.4.2.1 5 from the Gansu Province line on the Lanzhou-Urumqi 19. Superoxide dismu- Rd., then 9.0 km NE on dirt road to Mirowlu, Hami tase SOD 1.15.1.1 2 (Kumul) Prefecture, Xinjiang Uygur Autonomous Re- a Electrophoretic conditions: (1) Amine–citrate (morpholine) pH gion, China.
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