Abstract
Tilapia is one of most important foodfish species. The low omega-3 to omega-6 fatty acid ratio in freshwater tilapia meat is disadvantageous for human health. Increasing omega-3 content is an important task in breeding to increase the nutritional value of tilapia. However, conventional breeding to increase omega-3 content is difficult and slow. To accelerate the increase of omega-3 through marker-assisted selection (MAS), we conducted QTL mapping for fatty acid contents and profiles in a F2 family of saline tilapia generated by crossing red tilapia and Mozambique tilapia. The total omega-3 content in F2 hybrid tilapia was 2.5 ± 1.0 mg/g, higher than that (2.00 mg/g) in freshwater tilapia. Genotyping by sequencing (GBS) technology was used to discover and genotype SNP markers, and microsatellites were also genotyped. We constructed a linkage map with 784 markers (151 microsatellites and 633 SNPs). The linkage map was 2076.7 cM long and consisted of 22 linkage groups. Significant and suggestive QTL for total lipid content were mapped on six linkage groups (LG3, -4, -6, -8, -13, and -15) and explained 5.8–8.3% of the phenotypic variance. QTL for omega-3 fatty acids were located on four LGs (LG11, -18, -19, and -20) and explained 5.0 to 7.5% of the phenotypic variance. Our data suggest that the total lipid and omega-3 fatty acid content were determined by multiple genes in tilapia. The markers flanking the QTL for omega-3 fatty acids can be used in MAS to accelerate the genetic improvements of these traits in salt-tolerant tilapia.
Similar content being viewed by others
References
Betancor M, Olsen RE, Solstorm D, Skulstad OF, Tocher DR (2016) Assessment of a land-locked Atlantic salmon (Salmo salar L.) population as a potential genetic resource with a focus on long-chain polyunsaturated fatty acid biosynthesis. Biochim Biophys Acta 1861(3):227–238
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(1):911–917
Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S (2014) The genomic substrate for adaptive radiation in African cichlid fish. Nature 513(7518):375–381
Castell J (1979) Review of lipid requirements of finfish. In: Halver, Tiews K (eds) Finfish nutrition and fishfeed technology. Heenemann Verlagsgesellschaft, Hamburg
Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3 (Bethesda) 1(3):171–182
Chauke E, Cukrowska E, Thaela-Chimuka MJ, Chimuka L, Nsengimana H, Tutu H (2008) Fatty acids composition in South African freshwater fish as indicators of food quality. Water SA 34:119–125
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138(3):963–971
Derayat A, Houston R, Guy D, Hamilton A, Ralph J, Spreckley N, Taggart J, Mcandrew B, Haley C (2007) Mapping QTL affecting body lipid percentage in Atlantic salmon (Salmo salar). Aquaculture 272:S250–S251
El-Sayed A-FM (2006) Tilapia culture. CABI, Cambridge
Holub DJ, Holub BJ (2004) Omega-3 fatty acids from fish oils and cardiovascular disease. Mol Cell Biochem 263(1/2):217–225
Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135(1):205–211
Karamichou E, Richardson RI, Nute GR, Gibson KP, Bishop SC (2006) Genetic analyses and quantitative trait loci detection, using a partial genome scan, for intramuscular fatty acid composition in Scottish blackface sheep. J Anim Sci 84(12):3228–3238
Karapanagiotidis IT, Bell MV, Little DC, Yakupitiyage A (2007) Replacement of dietary fish oils by alpha-linolenic acid-rich oils lowers omega 3 content in tilapia flesh. Lipids 42(6):547–559
Karapanagiotidis IT, Bell MV, Little DC, Yakupitiyage A, Rakshit SK (2006) Polyunsaturated fatty acid content of wild and farmed tilapias in Thailand: effect of aquaculture practices and implications for human nutrition. J Agric Food Chem 54(12):4304–4310
Kocher TD, Lee W-J, Sobolewska H, Penman D, Mcandrew B (1998) A genetic linkage map of a cichlid fish, the tilapia (Oreochromis niloticus). Genetics 148(3):1225–1232
Kuang Y, Zheng X, Lv W, Cao D, Sun X (2015) Mapping quantitative trait loci for flesh fat content in common carp (Cyprinus carpio). Aquaculture 435:100–105
Lander E, Kruglyak L (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11(3):241–247
Leaver MJ, Taggart JB, Villeneuve L, Bron JE, Guy DR, Bishop SC, Houston RD, Matika O, Tocher DR (2011) Heritability and mechanisms of n-3 long chain polyunsaturated fatty acid deposition in the flesh of Atlantic salmon. Comp Biochem Physiol Part D Genomics Proteomics 6(1):62–69
Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Prepr 1303.3997
Li HL, Gu XH, Li BJ, Chen CH, Lin HR, Xia JH (2017) Genome-wide QTL analysis identified significant associations between hypoxia tolerance and mutations in the GPR132 and ABCG4 genes in Nile tilapia. Mar Biotechnol 19:442–453
Lien S, Gidskehaug L, Moen T, Hayes BJ, Berg PR, Davidson WS, Omholt SW, Kent MP (2011) A dense SNP-based linkage map for Atlantic salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics 12(1):615
Lin G, Chua E, Orban L, Yue GH (2016) Mapping QTL for sex and growth traits in salt-tolerant tilapia (Oreochromis spp. × O. mossambicus). PLoS One 11(11):e0166723
Liu F, Sun F, Li J, Xia JH, Lin G, Tu RJ, Yue GH (2013) A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus × Oreochromis spp.) and mapping of sex-determining loci. BMC Genomics 14(1):58
Liu F, Sun F, Xia JH, Li J, Fu GH, Lin G, Tu RJ, Wan ZY, Quek D, Yue GH (2014) A genome scan revealed significant associations of growth traits with a major QTL and GHR2 in tilapia. Sci Rep 4:7256
Liu P, Wang L, Wan ZY, Ye BQ, Huang S, Wong S-M, Yue GH (2016a) Mapping QTL for resistance against viral nervous necrosis disease in Asian seabass. Mar Biotechnol 18(1):107–116
Liu S, Li Y, Qin Z, Geng X, Bao L, Kaltenboeck L, Kucuktas H, Dunham R, Liu Z (2016b) High-density interspecific genetic linkage mapping provides insights into genomic incompatibility between channel catfish and blue catfish. Anim Genet 47(1):81–90
Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11(1):31–46
Negrín-Báez D, Navarro A, Rodríguez-Ramilo ST, Afonso JM, Zamorano MJ (2016) Identification of quantitative trait loci associated with the skeletal deformity LSK complex in gilthead seabream (Sparus aurata L.) Mar Biotechnol 18(1):98–106
Nguyen NH (2016) Genetic improvement for important farmed aquaculture species with a reference to carp, tilapia and prawns in Asia: achievements, lessons and challenges. Fish Fish 17(2):483–506
Nguyen NH, Ponzoni RW, Yee HY, Abu-Bakar KR, Hamzah A, Khaw HL (2010) Quantitative genetic basis of fatty acid composition in the GIFT strain of Nile tilapia (Oreochromis niloticus) selected for high growth. Aquaculture 309(1-4):66–74
O’fallon J, Busboom J, Nelson M, Gaskins C (2007) A direct method for fatty acid methyl ester synthesis: application to wet meat tissues, oils, and feedstuffs. J Anim Sci 85(6):1511–1521
Palaiokostas C, Bekaert M, Khan MG, Taggart JB, Gharbi K, Mcandrew BJ, Penman DJ (2013) Mapping and validation of the major sex-determining region in Nile tilapia (Oreochromis niloticus L.) using RAD sequencing. PLoS One 8(7):e68389
Perschbacher PW (2017) Tilapia in Intensive Co-culture. Wiley, Oxford
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7(5):e37135
Sanchez M-P, Iannuccelli N, Basso B, Bidanel J-P, Billon Y, Gandemer G, Gilbert H, Larzul C, Legault C, Riquet J, Milan D, Le Roy P (2007) Identification of QTL with effects on intramuscular fat content and fatty acid composition in a Duroc × Large White cross. BMC Genet 8(1):55
Sun Y-L, Jiang D-N, Zeng S, Hu C-J, Ye K, Yang C, Yang S-J, Li M-H, Wang D-S (2014) Screening and characterization of sex-linked DNA markers and marker-assisted selection in the Nile tilapia (Oreochromis niloticus). Aquaculture 433:19–27
Tocher DR (2015) Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective. Aquaculture 449:94–107
Van Ooijen JW (2004) MapQTL®5.0, software for the mapping of quantitative trait loci in experimental populations. Kyazma B.V, Wageningen
Van Ooijen JW (2006) JoinMap 4.0: software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen
Wang L, Bai B, Huang S, Liu P, Wan ZY, Ye B, Wu J, Yue GH (2017a) QTL mapping for resistance to iridovirus in Asian seabass using genotyping-by-sequencing. Mar Biotechnol 19(5):517–527
Wang L, Bai B, Liu P, Huang SQ, Wan ZY, Chua E, Ye B, Yue GH (2017b) Construction of high-resolution recombination maps in Asian seabass. BMC Genomics 18(1):63
Wang M, Lu M (2016) Tilapia polyculture: a global review. Aquac Res 47(8):2363–2374
Xia JH, Bai Z, Meng Z, Zhang Y, Wang L, Liu F, Jing W, Wan ZY, Li J, Lin H (2015) Signatures of selection in tilapia revealed by whole genome resequencing. Sci Rep 5:14168
Xia JH, Lin G, He X, Yunping B, Liu P, Liu F, Sun F, Tu R, Yue GH (2014a) Mapping quantitative trait loci for omega-3 fatty acids in Asian seabass. Mar Biotechnol 16(1):1–9
Xia JH, Wan ZY, Ng ZL, Wang L, Fu GH, Lin G, Liu F, Yue GH (2014b) Genome-wide discovery and in silico mapping of gene-associated SNPs in Nile tilapia. Aquaculture 432:67–73
Xu P, Xu J, Zhang Y, Feng J, Dong C, Jiang L, Feng J, Chen B, Gong Y, Chen L (2016) An ultra-high density linkage map and QTL mapping for sex and growth-related traits of common carp (Cyprinus carpio). Sci Rep 6:30101
Young K (2009) Omega-6 (n-6) and omega-3 (n-3) fatty acids in tilapia and human health: a review. Int J Food Sci Nutr 60(sup5):203–211
Yu Y, Zhang X, Yuan J, Wang Q, Li S, Huang H, Li F, Xiang J (2017) Identification of sex-determining loci in Pacific white shrimp Litopeneaus vannamei using linkage and association analysis. Mar Biotechnol 19(3):277–286
Yue G, Lin H, Li J (2016) Tilapia is the fish for next-generation aquaculture. Int J Marine Sci Ocean Technol 3:11–13
Yue G, Orban L (2002) Microsatellites from genes show polymorphism in two related Oreochromis species. Mol Ecol Resour 2(2):99–100
Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15(3):376–396
Yue GH, 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
Acknowledgements
Professor Valerie C. L. Lin is deeply appreciated for her support with this project that is part of Grace Lin’s PhD thesis. We thank our colleague Mr. Baoqing Ye for English editing of the manuscript.
Funding
This research was supported by the National Research Foundation, Prime Minister’s Office, Singapore, under its Competitive Research Program (CRP Award No. NRF-CRP7-2010-01)
Author information
Authors and Affiliations
Corresponding authors
Electronic Supplementary Material
Supplementary Fig. 1
(DOCX 9604 kb)
Supplementary Figures 2–4 QTL for omega-3 content
(DOCX 361 kb)
Supplementary Table 1
(DOCX 32 kb)
Supplementary Table 2
(XLS 201 kb)
Rights and permissions
About this article
Cite this article
Lin, G., Wang, L., Ngoh, S.T. et al. Mapping QTL for Omega-3 Content in Hybrid Saline Tilapia. Mar Biotechnol 20, 10–19 (2018). https://doi.org/10.1007/s10126-017-9783-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-017-9783-3