Development and potential application of new set of Atlantic bluefin tuna EST-SSRs in the survival success during farming cycle


IVANA RADONIĆ
https://orcid.org/0000-0002-3718-5761
ŽELJKA TRUMBIĆ
https://orcid.org/0000-0001-9082-5871
TANJA ŠEGVIĆ- BUBIĆ
LEON GRUBIŠIĆ
IVONA MLADINEO
Resumen

The capture-based aquaculture of the Atlantic bluefin tuna (Thunnus thynnus) starts with the catch of wild individuals, a slow-operating transport to the rearing facilities, introduction to rearing cages, and adaptation to the captive environment; all bearing significant risks for the onset of stressful conditions that consequently can result in unexpected mortalities.

In order to explore whether the survival success through the farming cycle might be monitored at the genetic level and linked to several immunity and stress response associated genes, we have developed a new set of 13 EST-SSRs for T. thynnus and subsequently analysed 334 samples of juvenile wild-caught tuna and captive-reared adults during two consecutive farming cycles in the Adriatic Sea.

The results evidenced a low FST value (0.005) with similar allele frequencies and no major allele loss between investigated groups. Two tested approaches for the identification of loci under selection did not indicate departure from neutrality for any of the 13 EST-SSRs, suggesting that the latter could not be considered adaptive in the studied context.

Our results are in agreement with other studies that attempted to detect adaptive signals in T. thynnus, stressing the problem associated with the sampling design of a species with complex migratory behavior, reproduction and particular zootechnical practices employed at the farms. Nonetheless, characteristics of 13 new polymorphic loci reported here contribute to the broadening of the existing EST-SSRs resource, being a useful asset in future genetic studies of T. thynnus.

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Albaina, A., Iriondo, M., Velado, I., Laconcha, U., Zarraonaindia, I. et al., 2013. Single nucleotide polymorphism discovery in albacore and Atlantic bluefin tuna provides insights into worldwide population structure. Animal Genetics, 44, 678-692.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., Lipman, D. J., 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
Antao, T., Lopes, A., Lopes, R. J., Beja-Pereira, A., Luikart, G., 2008. LOSITAN, A workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics, 9, 1-5.
Antoniou, A., Kasapidis, P., Kotoulas, G., Mylonas, C. C., Magoulas, A., 2017a. Genetic diversity of Atlantic Bluefin tuna in the Mediterranean Sea, insights from genome-wide SNPs and microsatellites. Journal of Biological Research (Thessalonike, Greece), 24 (3),1-14.
Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H. et al., 2000. Gene Ontology, tool for the unification of biology. Nature Genetics, 25, 25-29.
Block, B.A., Teo, S. L. H., Walli, A., Boustany, A., Stokesbury, M.J.W. et al., 2005. Electronic tagging and population structure of Atlantic bluefin tuna. Nature, 434, 1121-1127.
Borstnik, B., Pumpernik, D., 2002. Tandem Repeats in Protein Coding Regions of Primate Genes. Genome Research, 12, 909-915.
Boustany, A.M., Reeb, C.A., Block, B. A. 2008. Mitochondrial DNA and electronic tracking reveal population structure of Atlantic bluefin tuna (Thunnus thynnus). Marine Biology, 156, 13-24.
Broughton, R.E., Gold, J.R., 1997. Microsatellite development and survey of variation in northern bluefin tuna (Thunnus thynnus). Molecular Marine Biology and Biotechnology, 6, 308-314.
Buentello, A., Seoka, M., Kato, K., Partridge, G.J., 2016. Tuna Farming in Japan and Mexico. p. 189-215. In, Advances in Tuna Aquaculture, Benetti, D. D., Patridge, G.J., Buentello, A., (Eds). Academic Press is an imprint of Elsevier. Oxford.
Carlson, M. 2018., org.Dr.eg.db, Genome wide annotation for Zebrafish. R package version 3.6.0.
Carlsson, J., McDowell, J.A.N., Diaz- Jaimes, P., Carlsson, J.E., Boles, S.B. et al., 2004. Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thunnus thynnus thynnus) population structure in the Mediterranean Sea. Molecular Ecology, 13, 3345-3356.
Carlsson, J., McDowell, J.R., Carlsson, J.E.L., Graves, J.E., 2007. Genetic identity of YOY bluefin tuna from the Eastern and Western Atlantic spawning areas. Journal of Heredity, 98, 23-28.
Carlsson, J., Gauthier, D.T., Carlsson, J.E.L., Coughlan, J.P., Dillane, E. et al., 2013. Rapid, economical single-nucleotide polymorphism and microsatellite discovery based on de novo assembly of a reduced representation genome in a non-model organism, a case study of Atlantic cod Gadus morhua, novel SNPs and microsatellites in Gadus morhua. Journal of Fish Biology, 82, 944-958.
Cerdà, J., Manchado, M., 2013. Advances in genomics for flatfish aquaculture. Genes & Nutrition, 8, 5-17.
Chapuis, M.P., Estoup, A., 2007. Microsatellite Null Alleles and Estimation of Population Differentiation. Molecular Biology and Evolution, 24, 621-631.
Chistiakov, D.A., Hellemans, B., Volckaert, F.A.M., 2006a. Microsatellites and their genomic distribution, evolution, function and applications, A review with special reference to fish genetics. Aquaculture, 255, 1-29.
Clark, T.B., Ma, L., Saillant, E., Gold, J.R., 2004. Microsatellite DNA markers for population-genetic studies of Atlantic bluefin tuna (Thunnus thynnus thynnus) and other species of genus Thunnus. Molecular Ecology Resources, 4, 70-73.
Cuéllar-Pinzón, J., Presa, P., Hawkins, S.J., Pita, A., 2016. Genetic markers in marine fisheries, Types, tasks and trends. Fisheries Research, 173, 194-205.
Dewoody, J., Nason, J.D., Hipkins, V.D., 2006 Mitigating scoring errors in microsatellite data from wild populations. Molecular Ecology Notes, 6, 951-957.
Earl, D.A., vonHoldt, B.M., 2012. Structure Harvester, a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
Ellis, J.R., Burke, J.M., 2007. EST-SSRs as a resource for population genetic analyses. Heredity, 99, 125-132.
Evans, D.L. 2015. Stress and immune responses of ranched southern bluefin tuna (Thunnus maccoyii castleneau). PhD Thesis. University of Tasmania. 124 pp.
Excoffier, L., Lischer H.L.E., 2010. Arlequin suite ver. 3.5, a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10 (3), 564-567.
Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data, linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
Foll, M., 2012. BayeScan v2. 1 user manual. Ecology, 20, 1450-1462.
Gemayel, R., Vinces, M.D., Legendre, M., Verstrepen, K.J., 2010. Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics, 44, 445-477.
Goudet, J. 2002. FSTAT version 2.9.3.2, a program to estimate and test gene diversities and fixation indices. Available online, http//www2.unil.ch/popgen/softwares/fstat.htm.
ICCAT, 2017. International Commission for the Conservation of Atlantic Tunas. Available online, https//www.iccat.int/en/#
Iseli, C., Jongeneel, C.V., Bucher, P., 1999. ESTScan, A program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. International Conference on Intelligent Systems for Molecular Biology, 138-148.
Jeffreys, H., 1998. Theory of probability. Oxford classic texts in the physical sciences. Clarendon Press; Oxford University Press, Oxford [Oxfordshire], New York. 459 pp.
Ji, P., Zhang, Y., Li, C., Zhao, Z., Wang, J., Li, J., Xu, P., et al. 2012. High throughput mining and characterization of microsatellites from common carp genome. International Journal of Molecular Sciences, 13, 9798-9807.
Jombart, T. 2008. Adegenet, a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
Ju, Z., Wells, M.C., Martinez, A., Hazlewood, L., Walter, R.B., 2005. An in silico mining for simple sequence repeats from expressed sequence tags of zebrafish, medaka, Fundulus, and Xiphophorus. In Silico Biology, 5, 439-463.
Katavic, I., Franicevic, V., Ticina, V., 2003. Rearing of small bluefin tunas (Thunnus thynnus L.) in the Adriatic Sea Preliminary study. Cashiers Options Mediterraneennes, 60, 95-99.
Kirchhoff, N.T., 2012. Health and performance of ranched southern bluefin tuna. PhD Thesis. University of Tasmania, 183 pp.
Laird, P.W., Zijderveld, A., Linders, K., Rudnicki, M.A., Jaenisch, R. et al., 1991. Simplified mammalian DNA isolation procedure. Nucleic Acids Research, 19, 4293.
Li, Y.C., Korol, A.B., Fahima, T., Beiles, A., Nevo, E., 2002. Microsatellites, genomic distribution, putative functions and mutational mechanisms, a review. Molecular Ecology, 11, 2453-2465.
Li, Y.C., 2004. Microsatellites within genes, structure, function, and evolution. Molecular Biology and Evolution, 21, 991-1007.
Liu, Z.J., Cordes, J.F., 2004. DNA marker technologies and their applications in aquaculture genetics. Aquaculture, 238, 1-37.
Louro, B., Passos, A.L.S., Souche, E.L., Tsigenopoulos, C., Beck, A. et al., 2010. Gilthead sea bream (Sparus auratus) and European sea bass (Dicentrarchus labrax) expressed sequence tags, characterization, tissue-specific expression and gene markers. Marine Genomics, 3, 179-191.
Magnadóttir, B., 2006. Innate immunity of fish (overview). Fish & Shellfish Immunology, 20, 137-151.
Metzgar, D., Bytof, J., Wills, C. 2000. Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Research, 10, 72-80.
Meyer, F. P. 1991. Aquaculture disease and health management. Journal of Animal Science, 69, 4201-4208.
Miyake, P., De la Serna, J., Di Natale, F., 2003. General review of bluefin tuna farming in the Mediterranean area. Collective Volumes of Scientific Papers ICCAT, 55, 114-124.
Miyashita, S., Sawada, Y., Hattori, N., Nakatsukasa, H., Okada, T. et al., 2000. Mortality of northern bluefin tuna Thunnus thynnus due to trauma caused by collision during growout culture. Journal of the World Aquaculture Society, 31, 632-639.
Mladineo, I., Miletić, I., Bočina, I., 2006. Photobacterium damselae subsp. piscicida Outbreak in Cage-Reared Atlantic Bluefin Tuna Thunnus thynnus. Journal of Aquatic Animal Health, 18, 51-54.
Morin, P.A., Leduc, R.G., Archer, F.I., Martien, K.K., Huebinger, R. et al., 2009. Significant deviations from Hardy-Weinberg equilibrium caused by low levels of microsatellite genotyping errors: technical advances. Molecular Ecology Resources, 9, 498-504.
Mylonas, C.C., De La Gándara, F., Corriero, A., Ríos, A.B., 2010. Atlantic bluefin tuna (Thunnus thynnus) farming and fattening in the Mediterranean Sea. Reviews in Fisheries Science, 18, 266-280.
Nakada, M., 2008. Capture-based aquaculture, global overview. FAO fisheries technical paper. Food and Agriculture Organization of the United Nations, Rome. 298 pp.
Neff, B.D., Fu, P., Gross, M.R. 2000. Microsatellite multiplexing in fish. Transactions of the American Fisheries Society, 129, 584-593.
Nikolic, N., Duthoy, S., Destombes, A., Bodin, N., West, W. et al., 2015. Discovery of genome-wide microsatellite markers in Scombridae, a pilot study on albacore tuna. PloS One, 10, 1-22.
Norris, A., Bradley, D., Cunningham, E., 1999. Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture, 180, 247-264.
Ottolenghi, F., 2008. Capture-based aquaculture, global overview. FAO fisheries technical paper. Food and Agriculture Organization of the United Nations, Rome, 298 pp.
Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
Rauta, P.R., Nayak, B., Das, S., 2012. Immune system and immune responses in fish and their role in comparative immunity study. A model for higher organisms. Immunology Letters, 148, 23-33.
Riccioni, G., Landi, M., Ferrara, G., Milano, I., Cariani, A., et al., 2010a. Spatio-temporal population structuring and genetic diversity retention in depleted Atlantic bluefin tuna of the Mediterranean Sea. Proceedings of the National Academy of Sciences, 107, 2102-2107.
Riccioni, G., Ferrara, G., Landi, M., Sella, M., 2010b. Spatio-temporal genetic patterns in Mediterranean bluefin tuna, population structuring and retention of genetic diversity. Collective Volumes of Scientific Papers ICCAT, 65, 996-1003.
Riccioni, G., Stagioni, M., Landi, M., Ferrara, G., Barbujani, G. et al., 2013. Genetic structure of bluefin tuna in the Mediterranean Sea correlates with environmental variables. Plos One, 8, 1-9.
Riccioni, G., Cariani, A., Ferrara, G., Cannas, R., Melis, R. et al. 2017. Evolutionary constraints limiting the variation of Expressed Sequence Tag-linked microsatellite loci, prevent the detection of local adaptation in Mediterranean Bluefin tuna. Fisheries Research, 190, 157-163.
Rice, P., Longden, I., Bleasby, A., 2000. EMBOSS, the European Molecular Biology Open Software Suite. Trends in genetics, 16, 276-277.
Rice, W.R., 1989. Analyzing Tables of Statistical Tests. Evolution, 43, 223.
Rooker, J.R., Alvarado Bremer, J.R., Block, B.A., Dewar, H., De Metrio, G. et al., 2007. Life history and stock structure of Atlantic bluefin tuna (Thunnus thynnus). Reviews in Fisheries Science, 15, 265-310.
Rooker, J., Arrizabalaga, H., Fraile, I., Secor, D., Dettman, D. et al., 2014. Crossing the line, migratory and homing behaviors of Atlantic bluefin tuna. Marine Ecology Progress Series, 504, 265-276.
Ryman, N., Palm, S., 2006. POWSIM, a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes, 6, 600-602.
Selkoe, K.A., Toonen, R.J., 2006 Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters, 9, 615-629.
Tautz, D., Renz, M., 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Research, 12, 4127-4138.
Taylor, N.G., McAllister, M.K., Lawson, G.L., Carruthers, T., Block, B.A., 2011. Atlantic bluefin tuna, a novel multistock spatial model for assessing population biomass. PloS One, 6, 1-10.
Tóth, G., Gáspári, Z., Jurka, J. 2000. Microsatellites in different eukaryotic genomes, survey and analysis. Genome Research, 10, 967-981.
Trumbić, Ž., Bekaert, M., Taggart, J.B., Bron, J.E., Gharbi, K. et al., 2015. Development and validation of a mixed-tissue oligonucleotide DNA microarray for Atlantic bluefin tuna, Thunnus thynnus (Linnaeus, 1758). BMC Genomics, 16, 1-17.
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C. et al., 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research, 40, 2-12.
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P. M., Shipley, P., 2004. micro-checker, software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
Vella, A., Vella, N., Karakulak, F.S., Oray, I., Garcia-Tiscar, S. et al., 2016. Population genetics of Atlantic bluefin tuna, Thunnus thynnus (Linnaeus, 1758), in the Mediterranean, implications for its conservation management. Journal of Applied Ichthyology, 32, 523-531.
Vinas, J., Gordoa, A., Fernández-Cebrián, R., Pla, C., Vahdet, Ü. et al., 2011. Facts and uncertainties about the genetic population structure of Atlantic bluefin tuna (Thunnus thynnus) in the Mediterranean. Implications for fishery management. Reviews in Fish Biology and Fisheries, 21, 527-541.
Waples, R.S., 2015. Testing for Hardy-Weinberg Proportions, Have We Lost the Plot? Journal of Heredity, 106, 1-19.
Ward, R.D., 1995. Population genetics of tunas. Journal of Fish Biology, 47, 259-280.
Wren, J.D., Forgacs, E., Fondon, J.W., Pertsemlidis, A., Cheng, S.Y. et al., 2000. Repeat Polymorphisms within Gene Regions, Phenotypic and Evolutionary Implications. The American Journal of Human Genetics, 67, 345-356.
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