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Molecular Evidence to Reconcile Taxonomic Instability in Mahseer Species (Pisces: Cyprinidae) of India

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Molecular Evidence to Reconcile Taxonomic Instability in Mahseer Species (Pisces: Cyprinidae) of India Org Divers Evol (2014) 14:307–326 DOI 10.1007/s13127-014-0172-8 ORIGINAL ARTICLE Molecular evidence to reconcile taxonomic instability in mahseer species (Pisces: Cyprinidae) of India Praveen Khare & Vindhya Mohindra & Anindya Sundar Barman & Rajeev Kumar Singh & Kuldeep Kumar Lal Received: 4 November 2013 /Accepted: 8 April 2014 /Published online: 19 May 2014 # Gesellschaft für Biologische Systematik 2014 Abstract The mahseers are an important group of fishes macrolepis and T. mosal mahanadicus, were not distinct from endemic to Asia with most species considered threatened. T. putitora (TrN+I+G 0.00). The high divergence with Conservation plans to save declining wild populations are mtDNA data failed to validate T. mosal mahanadicus as a hindered by unstable taxonomy, and detailed systematic re- subspecies of T. mosal (TrN+I+G 0.031). Morphological view could form a solid platform for future management and outliers discovered within the distribution range of Tor tor conservation. D-loop and cytochrome c oxidase I (COI) (TrN+I+G 0.022 to 0.025) shared the same lineage with mtDNA sequences were examined in nine mahseer species T. putitora (TrN+I+G 0.002 to 0.005), indicating a new of Tor, Neolissochilus,andNaziritor. Pseudogenes amplified extended distribution of the Himalayan mahseer T. putitora in a portion of the species limited the utility of the D-loop in the rivers of the Indian central plateau. The findings indicate region. ABGD analysis, NJ, ML, and MP methods and ge- the need for integrating molecular and morphological tools for netic distance (TrN+I+G) using COI data revealed concor- taxonomic revision of the Tor and Naziritor genera, so that dant species delimiting patterns. The three genera were mono- taxa are precisely defined for accurate in situ and ex situ phyletic, separated as distinct clades (TrN+I+G 0.064 to conservation decisions. 0.106), and Naziritor was flagged as a separate genus, distinct from Puntius (TrN+I+G 0.196). Out of seven nominal spe- Keywords Mahseer . Taxonomy . mtDNA . COI . D-loop . cies known for Tor cogeners from India, only five were Freshwater . Conservation recovered with mtDNA data (TrN+I+G 0.000 to 0.037) and two species could not be distinguished with the molecular data Abbreviations set employed. Tor mosal,synonymizedasTor putitora,was mtDNA Mitochondrial DNA rediscovered as a distinct species (TrN+I+G 0.031) based on COI Cytochrome c oxidase unit I its type locality. Tor mussulah was confirmed as a separate ABGD Automatic Barcode Gap Discovery species (TrN+I+G 0.019 to 0.026). Two valid species, Tor NJ Neighbor joining ML Maximum likelihood MP Maximum parsimony Electronic supplementary material The online version of this article TrN+I+G Tamura and Nei within variation site and (doi:10.1007/s13127-014-0172-8) contains supplementary material, gamma correction which is available to authorized users. HKY+G Hasegawa Kishino Yano + Gamma correction P. Khare : V.Mohindra : A. S. Barman : R. K. Singh : K. K. Lal (*) Ti/Tv Transition to transversion ratio National Bureau of Fish Genetic Resources, Canal Ring Road, Telibagh, Lucknow, U.P, India 226002 e-mail: [email protected] Introduction K. K. Lal e-mail: [email protected] Fishes of the genera Tor, Neolissochilus,andNaziritor (fam- ily: Cyprinidae; subfamily: Cyprininae), commonly known as A. S. Barman College of Fisheries, Central Agricultural University, Lembucharra, mahseers, are economically valued as sport fish, in capture Tripura, India fisheries, and for aquaculture. Mahseers inhabit both rivers 308 P. Khare et al. and lakes, ascending to rapid streams with rocky bottoms due to combination of characters (Chen and Yang 2004)such (Desai 2003) and are distributed from the Middle East to as 3–3.5 (vs. 2.5) scales from lateral line to pelvic fin origin, South and Southeast Asia (Roberts 1999; Silas et al. 2005). shorter caudal peduncle length (13.0 % vs. 17.2 % of stan- This group of large-scaled carps is endemic to Asia. Mahseers dard length), lesser body depth (26.4 % vs. 24.0 % of stan- originated in southwest China and spread westward during the dard length) and longer caudal peduncle depth (12.0 % vs. Pliocene and thereafter spread south to the Malay Archipelago 10.9 % of standard length). and southwestward to the Indian peninsula and Sri Lanka In southern Asia, the Indian subcontinent harbors the (Shrestha 1997). The iconic mahseers are listed among the highest species richness for Tor; seven species are distributed 20 mega fishes of the world (Stone 2007). However, across the Himalayas and the central and Deccan plateaus overfishing, habitat degradation, and several anthropogenic (Desai 2003; Jayaram 2005). These are T. putitora factors are responsible for the decline of their natural popula- (Hamilton), T. tor (Hamilton), Tor khudree (Sykes), Tor tion (Pinder and Raghavan 2012). Of 18 mahseer species progeneius (McClelland), Tor mosal (Sykes), Tor mussullah assessed under the IUCN criteria, 10 are listed as threatened, (Sykes), and Tor kulkarnii (Menon). In a recent review on namely under the “endangered” and “vulnerable” categories Indian mahseers, Dinesh et al. (2010)acceptedonlyfivevalid (IUCN 2013). To improve the natural population distribution species based on morphological descriptions and ignored of mahseers, comprehensive conservation strategies, includ- T. mosal and T. kulkarni,aswellassomeofthenewlyreported ing habitat management, protection, and artificial propagation species such as Tor moyarensis and Tor remadevi. T. mosal are needed. Taxonomic stability of an organism is the essential has been considered a synonym of T. putitora (Froese and platform before developing conservation action plans Pauly 2013; Eschmeyer et al. 2013). Deccan mahseers, (Morrison et al. 2009) which unfortunately is likely to be a T. khudree,andT. mussulah, are exclusive to the rivers of large constraint for mahseer conservation. the Deccan plateau and peninsular India (Jayaram; 2005). Mahseer systematics has been a subject of considerable Three subspecies, T. mosal mahanadicus (David 1953a, b), interest to taxonomists, however, contradiction in nomencla- T. khudree malabaricus (Jerdon) from Peninsular India and ture, possibly due to plasticity of characters (Mohindra et al. T. khudree longispinus, are considered valid, were not con- 2007) is leading to taxonomic instability in this group of firmed by evidence based on recent molecular studies. species. Eschmeyer et al. (2013) catalogued a total of 59 T. khudree malabaricus has been characterized as a separate currently valid species belonging to the mahseer group with species, T. malabaricus (Silas et al. 2005).T.mosal 36 assigned to the genus Tor, 22 to the genus Neolissochilus, mahandicus (David 1953a, b), which is endemic to the and one under Naziritor. However, these numbers vary be- Mahanadi River that originates from the central plateau, is cause of the taxonomic uncertainties regarding this group also described as T. khudree mahanadicus (Menon 1992), (Siraj et al. 2007; Froese and Pauly 2013). Naziritor (Mirza T. tor mahanadicus (Sugunan 1995) and a synonym of and Javed 1985) was proposed to accommodate mahseer T. khudree. However, a RAPD profile of T. mosal species found in the Zhob River (Naziritor zhobensis)in mahanadicus found it to be more similar to T. putitora than West Pakistan and was represented by the single species until all other Tor species (Mohindra et al. 2007). Nguyen et al. Menon (1999) classified Tor chelynoides (Talwar and (2006) concluded that T. khudree longispinus could not be Jhingran 1991)asNaziritor chelynoides. However, currently, distinguished from T. khudree on the basis of three mitochon- this species is recognized as Puntius chelynoides (Dahanukar drial genes. 2010; Froese and Pauly 2013). Mahseers are generally present in the so called “Tor zone” Across their distribution in Asia, species of Tor are among (600–1,200 m) of the glacier-fed Himalayan Rivers (Singh the most diversified of the cyprinids, and taxonomists have and Kumar 2000) and have much greater reach to the lower conflicting opinions regarding their nomenclature because of reaches in the peninsular Indian rivers (Ajithkumar et al. the morphological variations that they exhibit (Silas et al. 1999).Thegoldenmahseer,T. putitora is the largest in size 2005). Tor putitora, the golden mahseer, is the most widely and is widely distributed in all Himalayan rivers and reported distributed in the trans-Himalayan rivers across south Asia to migrate up to an altitude of 2,000 msl (Raina et al. 1999). including Myanmar, Bhutan, Bangladesh, India, China, Currently, only T. tor is known to exist both in the rivers of Nepal, and Pakistan (Bhatt et al. 2004). In portions of its Himalayas and also those flowing through the central plateau, known range of distribution, new species were split from such as in Narmada, Tapti, and Tons (Desai 2003; Dinesh et al. T. putitora on the basis of certain discriminating morpholog- 2010).Laletal.(2013) described the extended distribution of ical characters, such as Tor macrolepis from the Indus river T. tor in the Godavari and Krishna peninsular rivers. system in Pakistan (Mirza and Awan 1976; Mirza 2004) The established morphological criteria, such as proportion based on the hypertrophied lip structure and Tor of head length to body depth (Talwar and Jhingran 1991; yingjiangensis from the upper Irrawadi basin in Yunan, Jayaram 2005;Laskaretal.2013) or lip and median lobe China. T. yingjiangensis was distinguished from T. putitora structure (Zhou and Cui
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