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Genetic diversity of sharpnose mullet Liza saliens introduced in southern Caspian Sea in comparison with one native Aegean Sea population

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Abstract

Sharpnose mullet, Liza saliens (Risso, 1810) is one of the valuable species in Caspian shoreline and it was first introduced to Caspian Sea from Black Sea between 1930 and 1934. In the present study, we used six microsatellite markers to obtain genetic information for L. saliens from four localities of southern Caspian Sea and for one native population from Greece coastline (northern Aegean Sea). Results showed lower number of alleles (Na = 5.7–6) and higher observed heterozygosity (Ho = 0.74–0.83) in Caspian Sea samples, related to the native Aegean population (Na = 8, Ho = 0.68). Significant deviations from Hardy-Weinberg expectations were detected in 19 out of 28 tests. Low genetic differentiation (provided Fst values) among samples was detected, but Behshahr sample was significantly differentiated from all the others. The UPGMA tree revealed three major clusters: the Behshahr sample and Greek population were clustered in two different clades, and the remaining three samples formed another cluster. The low genetic variation and spatial differentiation among Caspian Sea samples may be justified by the recent establishment.

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References

  • Abdoli, A., The Inland Water Fishes of Iran, Tehran: Tehran Wildl. Mus. Press, 1999.

    Google Scholar 

  • Amsellem, L., Noyer, J., Le Bourgeois, T., and Hossaert-McKey, M., Comparison of genetic diversity of the invasive weed Rubus alceifolius Poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers, Mol. Ecol., 2000, vol. 9, pp. 443–455. doi 10.1046/j.1365-294x.2000.00876.x

    Article  CAS  PubMed  Google Scholar 

  • Ayllon, F., Davaine, P., Beall, E., Martinez, J.L., and Garcia-Vazquez, E., Bottlenecks and genetic changes in Atlantic salmon (Salmo salar L.) stocks introduced in the Subantarctic Kerguelen Islands, Aquaculture, 2004, vol. 237, pp. 103–116. doi 10.1016/j.aquaculture.2004.04.014

    Article  Google Scholar 

  • Benbouza, H., Jacquemin, J.M., Baudoin, J.P., and Mergeai, G., Optimization of a reliable, fast, cheap and sensitive silver staining method to detect SSR markers in polyacrylamide gels, Biotechnol. Agron. Soc. Environ., 2006, vol. 10, no. 2, pp. 77–81. doi 10.1023/B:BIGI.0000034426.31105.

    CAS  Google Scholar 

  • da Berg, L.S., Freshwater Fishes of the USSR and Adjacent Countries, Jerusalem: Israel Progr. Sci. Transl., 1965.

    Google Scholar 

  • Bhassu, S., Yusoff, K., Panandam, J., Embong, W.K., Oyyan, S., and Tan, S.G., The genetic structure of Oreochromis spp. (tilapia) populations in Malaysia as revealed by microsatellite DNA analysis, Biochem. Genet., 2004, vol. 42, pp. 217–229. doi 10.1023/B:BIGI.0000034426.31105.

    Article  CAS  PubMed  Google Scholar 

  • da Borrell, Y.J., Bernardo, D., Blanco, G., Vázquez, E., and Sánchez, J.A., Spatial and temporal variation of genetic diversity and estimation of effective population sizes in Atlantic salmon (Salmo salar L.) populations from Asturias (Northern Spain) using microsatellites, Conserv. Genet., 2008, vol. 9, pp. 807–819. doi 10.1007/s10592-007-9400-5

    Article  Google Scholar 

  • Bruford, M.W. and Wayne, R.K., Microsatellites and their application to population genetic studies, Curr. Opin. Genet. Dev., 1993, vol. 3, pp. 939–943. doi 10.1016/0959-437X(93)90017-J

    Article  CAS  PubMed  Google Scholar 

  • Coad, B.W., Freshwater fishes of Iran, 2014. http://www.briancoad.com.

    Google Scholar 

  • Daryanabard, G.R., Evaluation of Some Biological Indicators of Bony Fish in the Southern Coasts of the Caspian Sea, Tehran: Iran. Fish. Res. Center, 2012, pp. 130.

    Google Scholar 

  • DeWoody, J. and Avise, J., Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals, J. Fish. Biol., 2000, vol. 56, no. 3, pp. 461–473. doi 10.1111/j.1095-8649.2000.tb00748.x

    Article  CAS  Google Scholar 

  • Dmitriev, A.N., Mullet in the Iranian waters of Caspian, Priroda (Moscow), 1964, no. 12, pp. 74–75.

    Google Scholar 

  • Ellegren, H., Microsatellite mutations in the germline: implications for evolutionary inference, Trends Genet., 2000, vol. 16, no. 12, pp. 551–558. doi 10.1016/S0168-9525(00)02139-9

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., Laval, G., and Schneider, S., Arlequin (version 3.0): an integrated software package for population genetics data analysis, Evol. Bioinf. Online, 2005, vol. 1, pp. 47–50.

    CAS  Google Scholar 

  • Fazli, H., Investigation of some biological characters of sharpnose mullet (Liza saliens) in south coastal of Caspian Sea, Iran. Sci. Fish. J., 1999, vol. 4, no. 1, pp. 29–42.

    Google Scholar 

  • Fazli, H. and Ghaninejad, D., Study of catch and some biological aspects of mugilid fish in southern Caspian Sea, Iran. Sci. Fish. J., 2004, vol. 13, no. 1, pp. 97–114.

    Google Scholar 

  • Genton, B.J., Shykoff, J.A., and Giraud, T., High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction, Mol. Ecol., 2005, vol. 14, no. 14, pp. 4275–4285. doi 10.1111/j.1365-294X.2005.02750.x

    Article  CAS  PubMed  Google Scholar 

  • Ghadirnejad, H. and Ryland, J.S., A study of food and feeding of grey mullets in the southern part of the Caspian Sea, Proc. Symp. on Feeding Ecology and Nutrition in Fish, MacKinlay, D. and Shearer, K., Eds., San Francisco, 1996, pp. 137–144.

    Google Scholar 

  • Ghaninejad, D., Moghim, M., and Fazli, H., Stock assessment of bony fishes of south coastal Caspian Sea, Iran. Sci. Fish. J., 1993, vol. 3, no. 1, pp. 35–52.

    Google Scholar 

  • Goudet, J., FSTAT a program to eastimate and test gene diversities and fixation indices, version 2.9.3, 2001. http://www2.unil.ch/popgen/softwares/fstat.html.

    Google Scholar 

  • Ha, H.P., Nguyen, T.T.T., Poompuang, S., and Na-Nakorn, U., Microsatellites revealed no genetic differentiation between hatchery and contemporary wild populations of striped catfish, Pangasianodon hypophthalmus (Sauvage 1878) in Vietnam, Aquaculture, 2009, vol. 291, pp. 154–160. doi 10.1016/j.aquaculture.2009.03.017

    Article  CAS  Google Scholar 

  • Hillis, D.M., Moritz, C., and Mable, B.K., Molecular Systematic, Sunderland: Sinauer, 1996.

    Google Scholar 

  • Khoroshko, A.I., Mullet, in Kaspiiskoe more: ikhtiofauna i promyslovye resursy (The Caspian Sea Ichthyofauna and Commercial Stocks), Moscow: Nauka, 1989.

    Google Scholar 

  • King, T., Kalinowski, S., Schill, W., Spidle, A., and Lubinski, B., Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation, Mol. Ecol., 2001, vol. 10, no. 4, pp. 807–821. doi 10.1046/j.1365-294X.2001.01231.x

    Article  CAS  PubMed  Google Scholar 

  • Kolbe, J.J., Glor, R.E., Schettino, L.R., Lara, A.C., Larson, A., and Losos, J.B., Genetic variation increases during biological invasion by a Cuban lizard, Nature, 2004, vol. 431, pp. 177–181. doi 10.1038/nature02807

    Article  CAS  PubMed  Google Scholar 

  • Lee, C.E., Evolutionary genetics of invasive species, Trends Ecol. Evol., 2002, vol. 17, pp. 386–391. doi 10.1016/S0169-5347(02)02554-5

    Article  Google Scholar 

  • Li, J., Wang, G., and Bai, Z., Genetic variability in four wild and two farmed stocks of the Chinese freshwater pearl mussel (Hyriopsis cumingii) estimated by microsatellite DNA markers, Aquaculture, 2009, vol. 287, pp. 286–291. doi 10.1016/j.aquaculture.2008.10

    Article  CAS  Google Scholar 

  • Lindholm, A.K., Breden, F., Alexander, H.J., Chan, W.-K., Thakurta, S.G., and Brooks, R., Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulate in Australia, Mol. Ecol., 2005, vol. 14, no. 12, pp. 3671–3682. doi 10.1111/j.1365-294X.2005.02697.x

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Chen, S., and Li, B., Assessing the genetic structure of three Japanese flounder (Paralichthys olivaceus) stocks by microsatellite markers, Aquaculture, 2005, vol. 243, pp. 103–111. doi 10.1016/j.aquaculture.2004.10.024

    Article  CAS  Google Scholar 

  • Lundrigan, T.A., Reist, J.D., and Ferguson, M.M., Microsatellite genetic variation within and among Arctic charr (Salvelinus alpinus) from aquaculture and natural populations in North America, Aquaculture, 2005, vol. 244, no. 1, pp. 63–75. doi 10.1016/j.aquaculture.2004.11.027

    Article  CAS  Google Scholar 

  • Marshall, T., Slate, J., Kruuk, L., and Pemberton, J., Statistical confidence for likelihood-based paternity inference in natural populations, Mol. Ecol., 1998, vol. 7, pp. 639–655. doi 10.1046/j.1365-294x.1998.00374.x

    Article  CAS  PubMed  Google Scholar 

  • Miggiano, E., Lyons, R.E., Li, Y., Dierens, L.M., Crosetti, D., and Sola, L., Isolation and characterization of microsatellite loci in the striped mullet, Mugil cephalus, Mol. Ecol. Notes, 2005, vol. 5, no. 2, pp. 323–326. doi 10.1111/j.1471-8286.2005.00915.x

    Article  CAS  Google Scholar 

  • Miller, M.P., Tools for population genetic analyses (TFPGA) 1.3. Windows program for the analysis of allozyme and molecular-population genetic data, ver. 1.3, 1997. http//www.bioweb.usu.edu/mpmbio.

    Google Scholar 

  • Mitton, J.B., Molecular markers and natural selection, NATO ASI Ser., Ser. A, 1998, pp. 225–241.

    Google Scholar 

  • Naderi, L., Shabani, A., and Imsiridou, A., Evaluation easy and reliable method to transfer DNA in long distance and time, Proc. 12th Iranian Genetics Congr., Tehran, 2012.

    Google Scholar 

  • Nei, M., Estimation of average heterozygosity and genetic distance from a small number of individuals, Genetics, 1978, vol. 89, no. 3, pp. 583–590.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nei, M., Maruyama, T., and Chakraborty, R., The bottleneck effect and genetic variability in populations, Evolution, 1975, vol. 29, pp. 1–10.

    Article  Google Scholar 

  • Norris, A.T., Bradley, D.G., and Cunningham, E.P., Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture, 1999, vol. 180, no. 3, pp. 247–264. 10.1016/S0044-8486(99)00212-4

    Article  Google Scholar 

  • Patimar, R., Some biological aspects of the sharpnose mullet Liza saliens (Risso, 1810) in Gorgan Bay–Miankaleh wildlife refuge (the Southeast Caspian Sea), Turk. J. Fish. Aquat. Sci., 2008, vol. 8, pp. 225–232.

    Google Scholar 

  • Peakall, R.O.D. and Smouse, P.E., Genalex 6, genetic analysis in Excel. Population genetic software for teaching and research, Mol. Ecol. Notes, 2006, vol. 6, pp. 288–295. doi 10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Pérez-Enciso, M. and Toro, M.A., Localización de Genes y Selección Mediante Marcadores Moleculares Genética y Genómica en Acuicultura. Publicaciones Científicas y Tecnológicas del Observatorio Español de Acuicultura, Espinosa de los Monteros, J., Ed., Madrid, 2007, pp. 361–400.

    Google Scholar 

  • Piry, S., Luikart, G., and Cornuet, J.M., BOTTLENECK, a computer program for detecting recent reductions in the effective population size using allele frequency data, J. Hered., 1999, vol. 90, pp. 502–503. doi 10.1093/jhered/90.4.502

    Article  Google Scholar 

  • Poorfaraj, V., Study of morphological and biological characteristics of the mullet fish in the southern coast of Caspian Sea, MSc Thesis, Tehran: Univ. of Tehran, 2006.

    Google Scholar 

  • Poulet, N., Balaresque, P., Aho, T., and Björklund, M., Genetic structure and dynamics of a small introduced population, the pikeperch, Sander lucioperca in the Rhône delta. Genetica, 2009, vol. 135, no. 1, pp. 77–86. doi 10.1007/s10709-008-9260-z

    Article  CAS  PubMed  Google Scholar 

  • Purcell, K.M., Ling, N., and Stockwell, C.A., Evaluation of the introduction history and genetic diversity of a serially introduced fish population in New Zealand, Biol. Invasions, 2012, vol. 14, pp. 2057–2065. doi 10.1007/s10530-014-0753-7

    Article  Google Scholar 

  • Purcell, K. and Stockwell, C., An evaluation of the genetic structure and post-introduction dispersal of a non-native invasive fish to the North Island of New Zealand, Biol. Invasions, 2015, vol. 17, pp. 625–636. doi 10.1007/s10530-012-0213-1

    Article  Google Scholar 

  • Quan, Y.C., Sun, X.W., and Liang, L.Q., Genetic polymorphism of microsatellite DNA in two populations of northern sheatfish (Silurus soldatovi), Acta Genet. Sin., 2006, vol. 33, pp. 908–916.

    Article  CAS  PubMed  Google Scholar 

  • Razavisayad, B., Stock management of economic bony fishes of Caspian Sea, Natl. Conf. on Suitable Exploitation of Aquatic Resources of Caspian Sea, Babolsar, 1990.

    Google Scholar 

  • Rezaei, M., Shabani, A., Shabanpour, B., and Kashiri, H., Microsatellites reveal weak genetic differentiation between Rutilus frisii kutum (Kamenskii, 1901) populations south of the Caspian Sea, Anim. Biol., 2011, vol. 61, pp. 469–483. doi 10.1163/157075511X597584

    Article  Google Scholar 

  • Roman, J. and Darling, J.A., Paradox lost, genetic diversity and the success of aquatic invasions, Trends Ecol. Evol., 2007, vol. 22, pp. 454–464. doi 10.1016/j.tree.2007.07.002

    Article  PubMed  Google Scholar 

  • Rousset, F. and Raymond, M., Testing heterozygote excess and deficiency, Genetics, 1995, vol. 140, pp. 1413–1419.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soltani, M. and Rahanandeh, M., Reported of bloat in mugil capito of Caspian Sea, J. Vet. Res., 2001, vol. 56, pp. 105–106.

    Google Scholar 

  • Triantafyllidis, A., Abatzopoulos, T.J., Leonardos, J., and Guyomard, R., Microsatellite analysis of the genetic population structure of native and translocated Aristotle’s catfish (Silurus aristotelis), Aquat. Living Resour., 2002, vol. 15, pp. 351–359. doi 10.1016/s0990-7440(02)01192-0

    Article  Google Scholar 

  • Tsitrone, A., Rousset, F., and David, P., Heterosis, marker mutational processes and population inbreeding history, Genetics, 2001, vol. 159, pp. 1845–1859.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waples, R., Separating the wheat from the chaff, patterns of genetic differentiation in high gene flow species, J. Hered., 1998, vol. 89, pp. 438–450. doi 10.1093/jhered/89.5.438

    Article  Google Scholar 

  • Wright, S., Evolution and the Genetics of Populations, Vol. 4: Variability within and among Natural Populations, Chicago: Univ. of Chicago Press, 1978.

    Google Scholar 

  • Xu, G., Shao, C., Liao, X., Tian, Y., and Chen, S., Isolation and characterization of polymorphic microsatellite loci from so-iuy mullet (Mugil soiuy Basilewsky 1855), Conserv. Genet., 2009, vol. 10, pp. 653–655. doi 10.1007/s10592-008-9602-5

    Article  CAS  Google Scholar 

  • Xu, Z., Primavera, J.H., de la Pena, L.D., Pettit, P., Belak, J., and Alcivar-Warren, A., Genetic diversity of wild and cultured black tiger shrimp (Penaeus monodon) in the Philippines using microsatellites, Aquaculture, 2001, vol. 199, pp. 13–40. doi 10.1016/S0044-8486(00)00535-4

    Article  CAS  Google Scholar 

  • Yeh, F.C., Yang, R.C., and Boyle, T., POPGENE Version 1.31. Microsoft Window-Bases Freeware for Population Genetic Analysis, Edmonton: Univ. of Alberta, 1999.

    Google Scholar 

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  1. Faculty of Fisheries and Environmental Sciences, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

    L. Naderi & A. Shabani

  2. Department of Fisheries and Aquaculture Technology, Alexander Technological Educational Institute of Thessaloniki, Thessaloniki, Greece

    A. Imsiridou

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  1. L. Naderi
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Naderi, L., Shabani, A. & Imsiridou, A. Genetic diversity of sharpnose mullet Liza saliens introduced in southern Caspian Sea in comparison with one native Aegean Sea population. J. Ichthyol. 57, 297–305 (2017). https://doi.org/10.1134/S0032945217020126

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