Shakeela PARVEEN, Khalid ABBAS, Muhammad AFZAL, Mumtaz HUSSAIN

Prediction of Potential Hybridization between Three Major Carps in Ravi River (Punjab, Pakistan) Basin by Using Microsatellite Markers

Three major carps namely; Labeo rohita, Catla catla, Cirrhinus mrigala are commercially important aquaculturefreshwater fish species of Pakistan. Ascertaining the pure species status of major carps is essential for their appropriatemanagement and conservation. The use of microsatellites DNA markers and Bayesian models based statistical methods haveconsiderably improved the estimation of admixture analyses at individual level. In the present study, a set of twelveheterologus microsatellite markers were employed to assess the extent of potential hybridization in stocks of major carpscollected from Ravi River basin. The methods, Structure assignation and Newhybrids status determination statistical analyseswere used to determine the status of pure and hybrid individuals. Multidimensional and model-based Bayesian assignmentanalyses consistently delineated the presence of individuals having mixed-ancestry genome and detected different levels ofhybridization between major carps fish species. The clustering analyses showed high efficiency in the detection of F1 hybridsas well as potential backcross specimens. For the first time, the incidence of natural hybridization between major carp fishspecies was detected on genetic basis, at frequency rates reaching about 7.77% in Ravi River basin Punjab, Pakistan. TheBayesian model statistical analyses proved to be robust tools in discriminating pure species and hybrid specimens.

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Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Zinner, D. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26(2), 229–246. http://dx.doi.org/10.1111/j.1420-9101.2012.02599.x

Allan, J. D., Abell, R., Hogan, Z., Revenga, C., Taylor, B. W., Welcomme, R. L., & Winemiller, K. (2005). Overfishing of inland waters. Bioscience, 55(12), 1041. http://dx.doi.org/10.1641/0006- 3568(2005)055[1041:Ooiw]2.0.Co;2

Allendorf, F. W., Leary, R. F., Spruell, P., & Wenburg, J. K. (2001). The problems with hybrids: setting conservation guidelines. Trends in Ecology & Evolution, 16(11), 613–622. http://dx.doi.org/10.1016/S0169-5347(01)02290-X

Anderson, E. C., & Thompson, E. A. (2002). A modelbased method for identifying species hybrids using multilocus data. Genetics, 160(3), 1217 –1229. http://dx.doi.org/test statistics; hybrids

Araki, H., Cooper, B., & Blouin, M. S. (2007). Genetic Effects of Captive Breeding Cause a Rapid, Cumulative Fitness Decline in the Wild. Science, 318(5847), 100–103. http://dx.doi.org/10.1126/science.1145621

Belkhir, K., Borsa, P., Goudet, J., Chikli, L. & Bonhomme, F. (2000). GENETIX, logiciel sous Windows TMpour la genetique des populations, version 4.01 University of Montpellier II, Montpellier.

Borrell, Y. J., Alvarez, J., Blanco, G., de Murguía, A. M., Lee, D., Fernández, C., … Prado, J. A. S. (2011). A parentage study using microsatellite loci in a pilot project for aquaculture of the European anchovy Engraulis encrasicolus L. Aquaculture, 310(3-4), 305– 311. http://dx.doi.org/10.1016/j.aquaculture.2010.10.025

Carlson, D. M., Pflieger, W. L., Trial, L., & Haverland, P. S. (1985). Distribution, biology and hybridization of Scaphirhynchus albus and S. platorynchus in the Missouri and Mississippi rivers. Environmental Biology of Fishes, 14(1), 51–59. http://dx.doi.org/10.1007/BF00001576

Carson, E. W., De la Maza-Benignos, M., de Lourdes Lozano-Vilano, M., Vela-Valladares, L., Banda- Villanueva, I., & Turner, T. F. (2014). Conservation genetic assessment of the critically endangered Julimes pupfish, Cyprinodon julimes. Conservation Genetics, 15(2), 483–488. http://dx.doi.org/10.1007/s10592-013-0548-x

Chauhan, T., & Rajiv, K. (2010). Molecular markers and their applications in fisheries and aquaculture. Advances in Bioscience and Biotechnology, 01(04), 281–291. http://dx.doi.org/10.4236/abb.2010.14037

Crooijmans, R. P. M. A., Poel, J. J. V., Groenen, M. A. M., Bierbooms, V. A. F., & Komen, J. (1997). Microsatellite markers in common carp (Cyprinus carpio L.). Animal Genetics, 28(2), 129–134. http://dx.doi.org/10.1111/j.1365-2052.1997.00097.x

Das, P., Mishra, A., & Srivastava, S. K. (1996). Status on research in applied carp genetics and breeding in India. Journal of Aquaculture in the Tropics, 11, 307- 318.

Docker, M. F., Dale, A., & Heath, D. D. (2003). Erosion of interspecific reproductive barriers resulting from hatchery supplementation of rainbow trout sympatric with cutthroat trout. Molecular Ecology, 12(12), 3515–3521. http://dx.doi.org/10.1046/j.1365-294X.2003.02000.x

Dudu, A., Suciu, R., Paraschiv, M., Georgescu, S. E., Costache, M., & Berrebi, P. (2011). Nuclear Markers of Danube Sturgeons Hybridization. International Journal of Molecular Sciences, 12(12), 6796–6809. http://dx.doi.org/10.3390/ijms12106796

Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology, 14(8), 2611–2620. http://dx.doi.org/10.1111/j.1365-294X.2005.02553.x

Excoffier, L., & Heckel, G. (2006). Computer programs for population genetics data analysis: a survival guide. Nature Reviews Genetics, 7(10), 745–758. http://dx.doi.org/10.1038/nrg1904

Ford, J. S., Myers, R. A., Palermo, V., Bailey, D., & Chen, D. (2008). A Global Assessment of Salmon Aquaculture Impacts on Wild Salmonids. PLoS Biology, 6(2), e33. http://dx.doi.org/10.1371/journal.pbio.0060033

Frankham, R. (2010). Where are we in conservation genetics and where do we need to go? Conservation Genetics, 11(2), 661–663. http://dx.doi.org/10.1007/s10592-009-0010-2

Goodman, S. J., Barton, N. H., Swanson, G., Abernethy, K., & Pemberton, J. M. (1999). Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics, 152(1), 355–71. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10224266

Gozlan, R. E., Britton, J. R., Cowx, I., & Copp, G. H. (2010). Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology, 76(4), 751–786. http://dx.doi.org/10.1111/j.1095-8649.2010.02566.x

Grady, J. M., & Cashner, R. C. (1988). Evidence of Extensive Intergeneric Hybridization among the Cyprinid Fauna of Clark Creek, Wilkinson Co., Mississippi. The Southwestern Naturalist, 33(2), 137. http://dx.doi.org/10.2307/3671888

Gunnell, K., Tada, M. K., Hawthorne, F. A., Keeley, E. R., & Ptacek, M. B. (2008). Geographic patterns of introgressive hybridization between native Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and introduced rainbow trout (O. mykiss) in the South Fork of the Snake River watershed, Idaho. Conservation Genetics, 9(1), 49–64. http://dx.doi.org/10.1007/s10592-007-9302-6

Hansen, M. M., Bekkevold, D., Jensen, L. F., Mensberg, K. L. D., & Nielsen, E. E. (2006). Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. Journal of Applied Ecology, 43(4), 669–679. http://dx.doi.org/10.1111/j.1365-2664.2006.01185.x

Hasselman, D. J., Argo, E. E., McBride, M. C., Bentzen, P., Schultz, T. F., Perez-Umphrey, A. A., & Palkovacs, E. P. (2014). Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Molecular Ecology, 23(5), 1137–1152. http://dx.doi.org/10.1111/mec.12674

Hoagstrom, C. W. (2015). Habitat loss and subdivision are additive mechanisms of fish extinction in fragmented rivers. Global Change Biology, 21(1), 4–5. http://dx.doi.org/10.1111/gcb.12578

Kamonrat, W., McConnell, S. K. J., & Cook, D. I. (2002). Polymorphic microsatellite loci from the Southeast Asian cyprinid, Barbodes gonionotus (Bleeker). Molecular Ecology Notes, 2(2), 89–90. http://dx.doi.org/10.1046/j.1471-8286.2002.00155.x

Konishi, M., Hosoya, K., & Takata, K. (2003). Natural hybridization between endangered and introduced species of Pseudorasbora, with their genetic relationships and characteristics inferred from allozyme analyses. Journal of Fish Biology, 63(1), 213–231. http://dx.doi.org/10.1046/j.1095-8649.2003.00146.x

Lajbner, Z., Linhart, O., & Kotlik, P. (2011). Human-aided dispersal has altered but not erased the phylogeography of the tench. Evolutionary Applications, 4(4), 545–561. http://dx.doi.org/10.1111/j.1752-4571.2010.00174.x

McDonald, D. B., Parchman, T. L., Bower, M. R., Hubert, W. A., & Rahel, F. J. (2008). An introduced and a native vertebrate hybridize to form a genetic bridge to a second native species. Proceedings of the National Academy of Sciences of the United States of America, 105(31), 10837–42. http://dx.doi.org/10.1073/pnas.0712002105

McGinnity, P., Prodöhl, P., Ferguson, A., Hynes, R., Maoiléidigh, N. O., Baker, N., … Cross, T. (2003). Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proceedings. Biological Sciences, 270(1532), 2443–50. http://dx.doi.org/10.1098/rspb.2003.2520

Mirza, M. R. and H. M. Sharif. 1996. A Key to fishes of the Punjab. Ilmi Kitab Khana. Lahore, Pakistan.

Nagpure, N. S., Kushwaha, B., Sriyastava, S. K., & Ponniah, A. A. G. (2001). Comparative cytogenetic studies in Indian major carps Labeo rohita, Catla catla and Cirrhinus mrigala (Cyprinidae, Pisces). Chromosome Science, 5, 153-158. http://ci.nii.ac.jp/els/110003723532.

Neff, N. A., & Smith, G. R. (1979). Multivariate Analysis of Hybrid Fishes. Systematic Biology, 28(2), 176–196. http://dx.doi.org/10.1093/sysbio/28.2.176

Nolte, A. W., Gompert, Z., & Buerkle, C. A. (2009). Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Molecular Ecology, 18(12), 2615–2627. http://dx.doi.org/10.1111/j.1365-294X.2009.04208.x

Padhi, B. K., & Mandal, R. K. (1997). Inadvertent hybridization in a carp hatchery as detected by nuclear DNA RFLP. Journal of Fish Biology, 50(4), 906–909. http://dx.doi.org/10.1111/j.1095-8649.1997.tb01985.x

Patel, A., Das, P., Swain, S. K., Meher, P. K., Jayasankar, P., & Sarangi, N. (2009). Development of 21 new microsatellite markers in Labeo rohita (rohu). Animal Genetics, 40(2), 253–254. http://dx.doi.org/10.1111/j.1365-2052.2008.01834.x

Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–59. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10835412

Rhymer, J. M., & Simberloff, D. (1996). Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27(1), 83–109. http://dx.doi.org/10.1146/annurev.ecolsys.27.1.83

Rundle, H. D., Nagel, L., Boughman, J. W., & Schluter, D. (2000). Natural selection and parallel speciation in sympatric sticklebacks. Science (New York, N.Y.), 287(5451), 306–8. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10634785

Sahu, B. P., Sahoo, L., Joshi, C. G., Mohanty, P., Sundaray, J. K., Jayasankar, P., & Das, P. (2014). Isolation and characterization of polymorphic microsatellite loci in Indian major carp, Catla catla using next-generation sequencing platform. Biochemical Systematics and Ecology, 57(57), 357–362. http://dx.doi.org/10.1016/j.bse.2014.09.010

Sato, M., Kawaguchi, Y., Nakajima, J., Mukai, T., Shimatani, Y., & Onikura, N. (2010). A review of the research on introduced freshwater fishes: new perspectives, the need for research, and management implications. Landscape and Ecological Engineering, 6(1), 99–108. http://dx.doi.org/10.1007/s11355-009-0086-3

Schemske, D. W. (2000). Understanding the origin of species. Evolution, 54(3), 1069–1073. http://dx.doi.org/10.1111/j.0014-3820.2000.tb00111.x

Scribner, K. T., Page, K. S., & Bartron, M. L. (2000). Hybridization in freshwater species: a review of case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries, 10, 293–323.

Senanan, W., Kapuscinski, A. R., Na-Nakorn, U., & Miller, L. M. (2004). Genetic impacts of hybrid catfish farming (Clarias macrocephalus×C. gariepinus) on native catfish populations in central Thailand. Aquaculture, 235(1-4), 167–184. http://dx.doi.org/10.1016/j.aquaculture.2003.08.020

Simonsen, V., Hansen, M. M., Mensberg, K.L. D., Sarder, R. I., & Alam, S. (2005). Widespread hybridization among species of Indian major carps in hatcheries, but not in the wild. Journal of Fish Biology, 67(3), 794– 808. http://dx.doi.org/10.1111/j.0022-1112.2005.00785.x

Tallmon, D., Luikart, G., & Waples, R. (2004). The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution, 19(9), 489–496. http://dx.doi.org/10.1016/j.tree.2004.07.003

Vandeputte, M., & Haffray, P. (2014). Parentage assignment with genomic markers: a major advance for understanding and exploiting genetic variation of quantitative traits in farmed aquatic animals. Frontiers in Genetics, 5, 432. http://dx.doi.org/10.3389/fgene.2014.00432

Verardi, A., Lucchini, V., & Randi, E. (2006). Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Molecular Ecology, 15(10), 2845–2855. http://dx.doi.org/10.1111/j.1365-294X.2006.02995.x

Whitney, K. D., Ahern, J. R., Campbell, L. G., Albert, L. P., & King, M. S. (2010). Patterns of hybridization in plants. Perspectives in Plant Ecology, Evolution and Systematics, 12(3), 175–182. http://dx.doi.org/10.1016/j.ppees.2010.02.002

Yue, G. H., & Orban, L. (2005). A simple and affordable method for high-throughput DNA extraction from animal tissues for polymerase chain reaction. Electrophoresis, 26(16), 3081–3083. http://dx.doi.org/10.1002/elps.200410411