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The Molecular Systematics of the Carasobarbus Species from Iran and Adjacent Areas, with Comments on Carasobarbus Albus (Heckel, 1843)

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The Molecular Systematics of the Carasobarbus Species from Iran and Adjacent Areas, with Comments on Carasobarbus Albus (Heckel, 1843) Environ Biol Fish (2011) 91:327–335 DOI 10.1007/s10641-011-9787-1 The molecular systematics of the Carasobarbus species from Iran and adjacent areas, with comments on Carasobarbus albus (Heckel, 1843) Kai Borkenhagen & Hamid Reza Esmaeili & Sasan Mohsenzadeh & Fatemeh Shahryari & Ali Gholamifard Received: 21 July 2010 /Accepted: 14 March 2011 /Published online: 14 April 2011 # Springer Science+Business Media B.V. 2011 Abstract The diversity of cytochrome b sequences of Introduction Carasobarbus species from Iran and adjacent areas was investigated. Two divergent haplotype groups were found Cyprinid fishes (Cyprinidae) are the major element of for C. luteus. The first one is widespread and congruent the Eurasian temperate freshwater fish fauna with with the biogeographical hypothesis of a recent isolation respect to abundance and species diversity (about 220 among the various populations as a consequence of genera and 2420 species worldwide; Nelson 2006). rising sea levels following the last Pleistocene glaciation. This complex group is characterised by considerable The second one is restricted to the Khabur River in Syria. morphological variability, which reflects the high The possibility that one of these groups corresponds to diversity of their habitats and ecological traits. In a C. albus is discussed, but we conclude that it is more recently updated list of freshwater fishes of Iran, 15 likely that C. luteus is a single species that retained two species of the Barbus s.l. group are listed (Coad 2010). divergent mitochondrial lineages. The mitochondrial Three of these belong to the genus Carasobarbus sequence diversity found for C. kosswigi and C. sublimus Karaman, 1971, namely C. luteus, C. kosswigi and is high, possibly due to small population size and C. sublimus. This genus is characterised by moderate consequent genetic drift. Carasobarbus kosswigi is body size, a smooth last unbranched dorsal-fin ray, paraphyletic with respect to C. sublimus, indicating a nine to ten (usually ten) branched dorsal-fin rays, recent speciation event of these taxa. six branched anal-fin rays and large scales with numerous parallel radii (Krupp 1985; Borkenhagen Keywords Cyprinidae . Carasobarbus luteus . 2005). Mitochondrial introgression . Biogeography. Carasobarbus luteus (Heckel, 1843), which is Cytochrome b . Middle East called himri in Iran, is widely distributed in the rivers Tigris and Euphrates and adjacent drainage basins. In Iran, it is found in the Tigris River Basin including the K. Borkenhagen (*) Hawr Al Azim Marsh, the Persian Gulf Basin Senckenberg Research Institute and Museum of Nature, including the Helleh, Dalaki, Shapur, Mond and Frankfurt, Germany e-mail: [email protected] Dasht-e Palang rivers and Lake Famur (Parishan), : : : the Lake Maharlu Basin and the Hormozgan Basin. It H. R. Esmaeili S. Mohsenzadeh F. Shahryari has been extirpated in the Quweiq in northern Syria. A A. Gholamifard few records from the Orontes in western Syria exist, but Department of Biology, College of Sciences, Shiraz University, its presence there is doubtful (Wossughi 1978; Bianco Shiraz, Iran and Bănărescu 1982;Krupp1985; Borkenhagen 328 Environ Biol Fish (2011) 91:327–335 2005; Coad 2010). Different populations vary in Materials and methods morphometric characters and colouration. Two other species and one subspecies were described, reflecting Specimens used in this study were collected from 20 this variation, but were later considered synonyms. localities including the Tigris-Euphrates System and the These are Systomus albus Heckel, 1843 from Orontes southern basins of Iran (Lake Famur and Qarah Agaj and Tigris, Systomus albus alpina Heckel, 1846 from River in the Gulf Basin, springs of Maharlu Basin and the Qarah Agaj and Lake Parishan and Barbus parie- springs of Hormuz Basin in southern Fars Province) schanica Wossughi, Khozahmat & Etemadfar, 1982 (Fig. 1) using electric fishing gear, cast nets and hook and from a river near Lake Parishan. line. Tissue samples were fixed in 96% ethanol. Voucher Carasobarbus kosswigi (Ladiges, 1960) occurs specimens are held in the Collections of the Biology across the Tigris-Euphrates System in Iraq, Syria Department, Shiraz University, Iran (CBSU) and the and Turkey. In Iran it inhabits the rivers Dez and Senckenberg Research Institute and Museum of Nature, Karkheh and their tributaries (Abdoli 2000; Coad Frankfurt, Germany (SMF). Additional acronyms refer to 2010). A closely related species, C. sublimus (Coad & the Institute of Hydrobiology, Chinese Academy of Najafpour, 1997) was described from the A’la River Sciences, Wuhan, China (IHBCAS), the National Muse- in Khuzestan (Tigris Basin) and subsequently reported um of Natural History Madrid, Spain (MNCN), the from the Persian Gulf Basin (Esmaeili et al. 2006). Natural History Museum Vienna, Austria (NMW) and The aim of this study was to assess genetic the Zoological Museum of Tel-Aviv University, Israel variation among Carasobarbus species and popula- (Tel-AvivZM). All specimens included in the molecular tions in Iran and adjacent countries. Our objective analysis are listed in Table 1. For taxonomic comparison was to compare the degree of genetic variation of the types of Systomus albus (NMW 53674-7 (4), NMW widespread vs. geographically restricted species, and 53680 (1), NMW 91400 (1), SMF 812 (1)), Systomus to explore potential relationships between ecological albus alpina (NMW 53678 (5), NMW 53679 (2), conditions, such as range size, and genetic diversity NMW 53681 (2), NMW 53682 (2)) and Systomus within evolutionary lineages. We were also interested luteus (NMW 10827 (1), NMW 54247 (2), NMW in how morphological and genetic variation within 54248 (1), NMW 54249 (1), NMW 54250 (2) NMW C. luteus compare, and evaluated the status of 54253 (2), NMW 54254 (3), NMW 54255 (2), NMW C. luteus relative to current synonymies. 80043 (2), SMF 6784 (1)) were studied. Fig. 1 Map of collection sites of C. canis (★), C. chantrei ( ), C. kosswigi ( ), C. luteus (✚) and C. sublimus ( ). Black symbols indicate samples from this study, grey sym- bols indicate localities of sequences from GenBank. The cross with four bars is the result of superposition of the two types of normal crosses Environ Biol Fish (2011) 91:327 Table 1 Material used in this study. Coordinates in brackets where inferred from locality names GenBank Collection No Species Locality Coordinates Collector Date Author Remark No. AF145944 – Carasobarbus Tigris R.–Diyarbakir, Turkey [37°54′39″N 40°14′12″E; 37°45′ ––Durand et al. luteus and Euphrates R.–Adiyaman, 50″N 38°16′40″E] 2002 Turkey AF145945 – ‘Barbus’ grypus Tigris R.–Diyarbakir, Turkey and [37°54′39″N 40°14′12″E; 37°45′ ––Durand et al. Euphrates R.–Adiyaman, Turkey 50″N 38°16′40″E] 2002 AF145947 – Carasobarbus Tiberias Lake, Israel [32°48′41″N 35°36′16″E] ––Durand et al. canis 2002 AF180852 – Carasobarbus Orontes R.–Antakya, Turkey [36°12"0″N 36°9′0″E] ––Durand et al. – chantrei 2002 335 AF180853 – Carasobarbus Tigris R.–Diyarbakir, Turkey [37°54′39″N 40°14′12″E] ––Durand et al. kosswigi 2002 AF180854 – ‘Barbus’ paytonii Oum Erbia River, Morocco [32°48′N 6°50′W] ––Durand et al. 2002 AF180855 – ‘Barbus’ harterti Sebou River, Morocco [34°04′N 5°33′W] ––Tsigenopoulos et al. 2010 AF180856 – ‘Barbus’ fritschii Sebou River, Morocco [34°04′N 5°33′W] ––Tsigenopoulos et al. 2010 AF287457 MNCN 92A Varicorhinus Oum Erbia, El Borj, Morocco [32°48′N 6°50′W] ––Machordom & maroccanus Doadrio 2001 AF288486 Tel-AvivZM Carasobarbus David River, Bet Shean, Israel [32°30′N 35°30′E] – Machordom and P11367 canis Doadrio 2001 AY463516 IHBCAS Neolissochilus Irrawaddy River Drainage, Tengchong, [25°01′N 98°29′E] ––He et al. 2004 uncatalogued heterostomus Yunnan Province, China FN821720 CBSU M125 Carasobarbus Bream bridge, Noor Abad, Fahlian 30°19′24.2″N 51°14′32.5″E H. R. Esmaeili 5 Oct this study luteus River, Zohreh River System, 2008 Gulf Basin, Iran FN821721 CBSU M129 Carasobarbus Khuzestan, Abbaran Village, 30°40′59.82″N 49°49′15.00″E H. Zareian 12 Sep this study luteus Maroon River, Jarahi, Tigris- 2008 Euphrates System, Iran FN821722 SMF 32889 Carasobarbus Balarud River, Khuzestan, Tigris- 32°35′19″N 48°17′11″E N. Alwan, K. 3 Mar this study luteus Euphrates System, Iran Borkenhagen 2008 FN821723 CBSU M127 Carasobarbus Faryab village, Mohr, Lamerd, 27°29′24.38″N 52°56′16.56″E A. Gholamifard 01 Jan this study luteus Fars, Mehran River, Hormuz 2008 Basin, Iran FN821724 CBSU M126 Carasobarbus Near Zali village, Kazeron, 29°31′41.2″N 51°46′25.0″E A. Gholamhosseini 10 Jan this study luteus Parishan lake, Gulf Basin, Iran 2008 FN821725 CBSU M128 Carasobarbus Simakan warm water spring, 28°36′31.62″N 53°08′46.62″E A. Gholamifard 10 Jan this study luteus Qarah Agaj River, Mond River 2008 System, Gulf Basin, Iran FN821726 CBSU M131 Carasobarbus Kaftarak, Shiraz, Maharlu lake, 29°33′21.0″N, 52°44′22.6″E A. Gholamhosseini 18 Nov this study luteus Maharlu Basin, Iran 2008 FN821727 SMF 30823 Carasobarbus Kheir Abad River, Gulf Basin, Iran 30°31′38.9″N 50°24′44.9″E K. Borkenhagen 6 Nov this study sublimus 2006 FN821728 SMF 30834 Carasobarbus Kheir Abad River, Gulf Basin, Iran 30°31′38.9″N 50°24′44.9″E K. Borkenhagen 6 Nov this study sublimus 2006 FN821729 SMF 30835 Carasobarbus Kheir Abad River, Gulf Basin, Iran 30°31′38.9″N 50°24′44.9″E K. Borkenhagen 6 Nov this study sublimus 2006 FN821730 SMF 31014 Carasobarbus Spring Golabii, 35 km north from 28°47.255′N 54°22.321′E J. Freyhof 2007 this study finclip luteus Darab, Hormuz Basin, Iran only 329 330 Table 1 (continued) GenBank Collection No Species Locality Coordinates Collector Date Author Remark No. FN821731 SMF 31017 Carasobarbus Spring Pirbanoo about 10 km 29°31.135′N 52°27.933′E J.
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