Marine Biotechnology

, Volume 20, Issue 1, pp 10–19 | Cite as

Mapping QTL for Omega-3 Content in Hybrid Saline Tilapia

  • Grace Lin
  • Le Wang
  • Si Te Ngoh
  • Lianghui Ji
  • Laszlo Orbán
  • Gen Hua Yue
Original Article


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.


Tilapia Omega-3 Breeding QTL MAS 



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 Information

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)

Supplementary material

10126_2017_9783_MOESM1_ESM.docx (9.4 mb)
Supplementary Fig. 1 (DOCX 9604 kb)
10126_2017_9783_MOESM2_ESM.docx (361 kb)
Supplementary Figures 2–4 QTL for omega-3 content (DOCX 361 kb)
10126_2017_9783_MOESM3_ESM.docx (32 kb)
Supplementary Table 1 (DOCX 32 kb)
10126_2017_9783_MOESM4_ESM.xls (202 kb)
Supplementary Table 2 (XLS 201 kb)


  1. 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):227–238CrossRefPubMedGoogle Scholar
  2. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(1):911–917CrossRefPubMedGoogle Scholar
  3. 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):375–381CrossRefPubMedPubMedCentralGoogle Scholar
  4. Castell J (1979) Review of lipid requirements of finfish. In: Halver, Tiews K (eds) Finfish nutrition and fishfeed technology. Heenemann Verlagsgesellschaft, HamburgGoogle Scholar
  5. 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):171–182CrossRefGoogle Scholar
  6. 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 34:119–125Google Scholar
  7. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138(3):963–971PubMedPubMedCentralGoogle Scholar
  8. 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–S251CrossRefGoogle Scholar
  9. El-Sayed A-FM (2006) Tilapia culture. CABI, CambridgeCrossRefGoogle Scholar
  10. Holub DJ, Holub BJ (2004) Omega-3 fatty acids from fish oils and cardiovascular disease. Mol Cell Biochem 263(1/2):217–225CrossRefGoogle Scholar
  11. Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135(1):205–211PubMedPubMedCentralGoogle Scholar
  12. 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):3228–3238CrossRefPubMedGoogle Scholar
  13. 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):547–559CrossRefPubMedGoogle Scholar
  14. 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):4304–4310CrossRefPubMedGoogle Scholar
  15. 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):1225–1232PubMedPubMedCentralGoogle Scholar
  16. 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 435:100–105CrossRefGoogle Scholar
  17. Lander E, Kruglyak L (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11(3):241–247CrossRefPubMedGoogle Scholar
  18. 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):62–69CrossRefPubMedGoogle Scholar
  19. Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Prepr 1303.3997Google Scholar
  20. 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 19:442–453Google Scholar
  21. 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):615CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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):e0166723CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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):58CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 4:7256CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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):107–116CrossRefPubMedGoogle Scholar
  26. 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):81–90CrossRefPubMedGoogle Scholar
  27. Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11(1):31–46CrossRefPubMedGoogle Scholar
  28. 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):98–106CrossRefPubMedGoogle Scholar
  29. 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):483–506CrossRefGoogle Scholar
  30. 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):66–74CrossRefGoogle Scholar
  31. 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):1511–1521CrossRefPubMedGoogle Scholar
  32. 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):e68389CrossRefPubMedPubMedCentralGoogle Scholar
  33. Perschbacher PW (2017) Tilapia in Intensive Co-culture. Wiley, OxfordCrossRefGoogle Scholar
  34. 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):e37135CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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):55CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 433:19–27CrossRefGoogle Scholar
  37. Tocher DR (2015) Omega-3 long-chain polyunsaturated fatty acids and aquaculture in perspective. Aquaculture 449:94–107CrossRefGoogle Scholar
  38. Van Ooijen JW (2004) MapQTL®5.0, software for the mapping of quantitative trait loci in experimental populations. Kyazma B.V, WageningenGoogle Scholar
  39. Van Ooijen JW (2006) JoinMap 4.0: software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, WageningenGoogle Scholar
  40. 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):517–527CrossRefPubMedGoogle Scholar
  41. 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):63CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wang M, Lu M (2016) Tilapia polyculture: a global review. Aquac Res 47(8):2363–2374CrossRefGoogle Scholar
  43. 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 5:14168CrossRefPubMedGoogle Scholar
  44. 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):1–9CrossRefPubMedGoogle Scholar
  45. 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 432:67–73CrossRefGoogle Scholar
  46. 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 6:30101CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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):203–211CrossRefPubMedGoogle Scholar
  48. 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):277–286CrossRefPubMedGoogle Scholar
  49. Yue G, Lin H, Li J (2016) Tilapia is the fish for next-generation aquaculture. Int J Marine Sci Ocean Technol 3:11–13Google Scholar
  50. Yue G, Orban L (2002) Microsatellites from genes show polymorphism in two related Oreochromis species. Mol Ecol Resour 2(2):99–100CrossRefGoogle Scholar
  51. Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15(3):376–396CrossRefGoogle Scholar
  52. 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):3081–3083CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Temasek Life Sciences Laboratory, 1 Research LinkNational University of SingaporeSingaporeSingapore
  2. 2.School of Biological SciencesNanyang Technological UniversitySingaporeSingapore
  3. 3.Department of Animal Sciences and Animal Husbandry, Georgikon FacultyUniversity of PannoniaKeszthelyHungary
  4. 4.Centre for Comparative GenomicsMurdoch UniversityMurdochAustralia
  5. 5.Department of Biological SciencesNational University of SingaporeSingaporeSingapore

Personalised recommendations