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Genetic and Morphometric Comparison of Two Isolated Populations of Barilius Bendelisis (Cypriniformes: Cyprinidae) from the Indian Himalayas

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Genetic and Morphometric Comparison of Two Isolated Populations of Barilius Bendelisis (Cypriniformes: Cyprinidae) from the Indian Himalayas Genetic and morphometric comparison of two isolated populations of Barilius bendelisis (Cypriniformes: Cyprinidae) from the Indian Himalayas Sumit Kumar & Deepak Singh* Freshwater Biodiversity Laboratory, Department of Zoology & Biotechnology, H.N.B. Garhwal Univesity, Srinagar (Garhwal), 246 174, Uttarakhand, India; [email protected] * Correspondence Received 05-IX-2018. Corrected 22-II-2018. Accepted 22-III-2019. Abstract: Barilius bendelisis (Hamilton) inhabits cold water drainages of the Himalayan region, occurring near the stream banks. It is an important component of the diet of rural population of Uttarakhand and Jammu. Despite the aquaculture importance of B. bendelisis, no extensive molecular characterization from two geo- graphically isolated rivers, Alaknanda and Chenab, has been conducted. In order to study those aspects, 567 samples of B. bendelisis were analysed and collected from these tributaries of two geographically isolated rivers between March of 2015 and April 2017. The morphometric data were analysed by means of truss analysis using tpsDig2 and PAST, whereas the genetic characterization was performed using the COI gene. In truss analysis 14 landmarks resulting in 90 measurements were studied from the digitized images of the sampled specimens. In total 23 measurements exhibited significant differences among the populations of B. bendelisis. The principal component analysis (PCA) generated seven components explaining- 93.15 % of total variance. Discriminant function analysis (DFA) revealed that 83.8 % of the specimens were classified into their original populations. Truss based morphometry and Maximum likelihood type of phylogenetic tree revealed heterogenicity between the two geographically isolated populations of B. bendelisis. Key words: Barilius bendelisis, truss analysis, PAST, Cypriniformes, morphometric characterization, molecular characterization. Kumar, S. & Singh, D. (2019). Genetic and morphometric comparison of two isolated populations of Barilius bendelisis (Cypriniformes: Cyprinidae) from the Indian Himalayas. Revista de Biología Tropical, 67(3), 466-477. Barilius bendelisis (Hamilton, 1807) com- Barilius bendelisis reaches a maximum monly called as “Indian hill trout” is a member length of 22.7 cm and is characterized by dark of the family Cyprinidae that occurs in shal- blue bars on the body, an elongated and com- low and cold waters of rivers and streams of pressed body and a dorsal fin inserted posterior the Himalayan region, northeastern India and to the mid length of the body (Rahman, 1989). several parts of Uttarakhand. This fish species Adults of Barilius bendelisis inhabit base hills is considered a fishery resource and also is streams and rivers with pebbles at bottom (Tal- found in the lentic and lotic water bodies where war & Jhingran, 1991; Menon, 1999). As per the exotic carp (Cyprinus carpio and Hypoph- IUCN (2012) the species has been placed as thalmichthys molitrix) and Indian major carp least concerned but in the future anthropogenic (Labeo. rohita, L. calbasu, L. bata, Cirrhinus activity, causing habitat destruction and over miragla and C. reba) cannot be raised success- exploitation are the main threats to this species. fully (Sahoo, Saikia, & Das, 2009). The overuse of B. bendelisis in the rural fishing 466 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(3): 466-477, June 2019 and aquarism is negatively impacting on its MATERIALS AND METHODS populations in the Himalayan region in the last years (Sah, Barat, Pande, Sati, & Goel, 2011). Collecting and identification of samples The species is mainly identified by means of The Chenab River is the largest tributary morphological features, which sometimes are of the Indus River of Western Himalaya while not useful to correctly identify all the exist- the Alaknanda River is the largest tributary ing populations because of its inherent high of Ganga River of Central Himalaya. Fresh variability (Victor, Hanner, Shivji, Hyde, & specimens of B. bendelisis were captured using Caldow, 2009). various fishing gears (cast nets, gill nets and Interspecific variation shown by using traditional Thali method) with the help of local COI barcodes in several studies is higher as fishermen from March 2015 to April 2017. A compared to the intraspecific variation (Hubert total of 267 specimens were collected from et al., 2008; Rock, Costa, & Walker, 2008; three different tributaries of the Chenab River Swartza, Mwalea, & Hanner, 2008; Steinke, Jhajjar, Dhudhar and Jhuni and 300 specimens Zemlak, & Hebert, 2009; Ward, Hanner, & were collected from other three tributaries of Hebert, 2009). The present study aimed at the Alaknanda River: Dugadda, Khankhra and to compare and illustrate morphometrics and Khandah Gad (Table 1). All the specimens molecular characters of Barilius bendelisis were collected before the breeding season and from the two geographically isolated tributaries after the spawning season. A solution of 10 % of Alaknanda and Chenab Rivers. of formalin was utilized to fix and preserve the In spite of high aquaculture scope, very collected samples that were morphometrically limited morphometric and molecular studies analysed. Some samples were stored in 95 % have been conducted for this fish species. The ethanol to perform the DNA analysis. The cap- tured specimens were identified with the help Truss Network Analysis overcomes the dis- of taxonomic keys of Day (1878), Talwar and advantages of manual morphometry and this Jhingran (1991), Mirza (1991), and Kullander, method produces a more systematic geometric Fang, Delling, and Ahlander (1999). The pres- characterization of fish shape and describes ent specimens of B. bendelisis were deposited inter-specific shape differences with high reso- in the museum of the Department of Zoology lution (Humphries et al., 1981; Strauss & and Biotechnology, HNB Garhwal University, Bookstein, 1982). Molecular characterization Srinagar (Garhwal). supports morphometric analysis. Therefore, the present study was designed to characterize Morphological analysis and compare the fish morphometrically and at molecular level from two isolated rivers of Digitalization of specimens: The speci- Western and Central Himalaya. mens were firstly cleaned in running water, TABLE 1 GPS coordinates and number of samples of Barilius bendelisis collected from the Indian Himalaya Sampling sites Variables Alaknanda River (Central Himalaya) Chenab River (Western Himalaya) Dugadda Khankhra Khandah Dhudhar Jhajjar Jhuni Latitude °N 30°15’31’’ 30°14’ 32’’ 30°11’47’’ 32°55’ 15’’ 32°52’ 25’’ 32°53’ 51’’ Longitude °E 78°43’7.89’’ 78°55’ 36’’ 78°46’ 34’’ 75°01’ 42’’ 74°59’ 54’’ 74°57’17’’ Number of samples collected 98 94 108 91 89 87 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 67(3): 466-477, June 2019 467 soaked by blotting paper and then placed on a correlation between transformed variables and flat platform with graph paper as background standard length was tested using SPSS and for digital images. To make the insertion points the results derived from the allometric method visible, the fins were erected and each indi- were confirmed (Turan, 1999). Ninety morpho- vidual was labelled with a specific code for metric characters were subjected to a univariate own identification. Photographs were taken by analysis of variance (ANOVA) to compare the means of a digital camera of (Nikon D3400). populations of the different sampled sites of To avoid errors during the image capture, all B. bendelisis. Then the significant variables photographs were taken by a single person (P < 0.05) were subjected to Factor analysis. from the same angle and height. A maximum likelihood method was used to extract the factors. The cumulative variance Truss analysis: A set of three software explained by the factors and loading of signifi- platforms, tpsUtil, tpsDig2 v2.1 (Rohlf, 2006) cant traits were retained. The retained factors and Paleontological Statistics (PAST) (Ham- were subjected to varimax rotation procedure to mer, Harper, & Ryan, 2001) was used to mea- identify the variables demonstrating high load- sure the truss distances of the digital images. ing for a given factor as described by Hatcher The truss analysis was based on 14 landmarks (1994). The Wilks l was used to compare the (Fig. 1) (Strauss & Bookstein, 1982; Mir, difference between all groups. Additionally, the Sarkar, Dwivedi, Gusain, & Jena, 2013). significant measurements were also subjected to the discriminant function analysis (DFA) to Statistical procedures: Size dependent calculate percentage of correctly classified fish. variation was conducted by using an allome- Statistical analysis for morphometric data were tric method suggested by Elliott, Haskard, performed using the SPSS vers.20 and Micro- and Koslow (1995) as “M = M (Ls/L0)b”, adj soft Excel 2007. where M is original measurement, Madj is the size adjusted measurement, L0 is the stan- dard length of the fish, Ls the overall mean DNA analysis standard length, and b was estimated for each character from the observed data as the slope Isolation of DNA, amplification and of the regression of log M on log L0 using all sequencing: Approximately 50 mg tissue was fish from every group. The significance of the used for genomic DNA isolation following Fig. 1. Schematic image of B. bendelisis showing the 14 landmarks used to compare among the populations. 1 tip of snout; 2 anterior border of eye; 3 posterior border of eye; 4 posterior border of operculum; 5 forehead (end of frontal bone);
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