Skip to main content

Advertisement

SpringerLink
Log in

High-Throughput Single Nucleotide Polymorphism (SNP) Discovery and Validation Through Whole-Genome Resequencing in Nile Tilapia (Oreochromis niloticus)

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Nile tilapia (Oreochromis niloticus) is the second most important farmed fish in the world and a sustainable source of protein for human consumption. Several genetic improvement programs have been established for this species in the world. Currently, the estimation of genetic merit of breeders is typically based on genealogical and phenotypic information. Genome-wide information can be exploited to efficiently incorporate traits that are difficult to measure into the breeding goal. Thus, single nucleotide polymorphisms (SNPs) are required to investigate phenotype–genotype associations and determine the genomic basis of economically important traits. We performed de novo SNP discovery in three different populations of farmed Nile tilapia. A total of 29.9 million non-redundant SNPs were identified through Illumina (HiSeq 2500) whole-genome resequencing of 326 individual samples. After applying several filtering steps, including removing SNP based on genotype and site quality, presence of Mendelian errors, and non-unique position in the genome, a total of 50,000 high-quality SNPs were selected for the development of a custom Illumina BeadChip SNP panel. These SNPs were highly informative in the three populations analyzed showing between 43,869 (94%) and 46,139 (99%) SNPs in Hardy-Weinberg Equilibrium; 37,843 (76%) and 45,171(90%) SNPs with a minor allele frequency (MAF) higher than 0.05; and 43,450 (87%) and 46,570 (93%) SNPs with a MAF higher than 0.01. The 50K SNP panel developed in the current work will be useful for the dissection of economically relevant traits, enhancing breeding programs through genomic selection, as well as supporting genetic studies in farmed populations of Nile tilapia using dense genome-wide information.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The sequence data used for SNP discovery and the 50K SNP chip developed here belongs to Aquainnovo/AquaChile, and it can be available upon reasonable request.

References

  • Bangera R, Correa K, Lhorente JP, Figueroa R, Yáñez JM (2017) Genomic predictions can accelerate selection for resistance against Piscirickettsia salmonis in Atlantic salmon (Salmo salar). BMC Genomics 18:121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baroiller JF, D’Cotta H (2001) Environment and sex determination in alligators. Comp Biochem Physiol C Toxicol Pharmacol 130:399–409

    Article  CAS  PubMed  Google Scholar 

  • Barria A, Marín-Nahuelpi R, Cáceres P et al (2019) Single-step genome-wide association study for resistance to Piscirickettsia salmonis in rainbow trout (Oncorhynchus mykiss). G3 (Bethesda). https://doi.org/10.1534/g3.119.400204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Berthelot C, Brunet F, Chalopin D et al (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5

  • Cáceres G, López ME, Cádiz MI et al (2019) Fine mapping using whole-genome sequencing confirms anti-Müllerian hormone as a major gene for sex determination in farmed Nile tilapia (Oreochromis niloticus L.). G3 (Bethesda). https://doi.org/10.1534/g3.119.400297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conte MA, Gammerdinger WJ, Bartie KL, Penman DJ, Kocher TD (2017) A high quality assembly of the Nile tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genomics 18:341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Correa K, Lhorente JP, López ME et al (2015) Genome-wide association analysis reveals loci associated with resistance against Piscirickettsia salmonis in two Atlantic salmon (Salmo salar L.) chromosomes. BMC Genomics 16:854

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Correa K, Lhorente JP, Bassini L et al (2016) Genome wide association study for resistance to Caligus rogercresseyi in Atlantic salmon (Salmo salar L.) using a 50K SNP genotyping array. Aquaculture. https://doi.org/10.1016/j.aquaculture.2016.04.008

    Article  CAS  Google Scholar 

  • Correa K, Bangera R, Figueroa R, Lhorente JP, Yáñez JM (2017) The use of genomic information increases the accuracy of breeding value predictions for sea louse (Caligus rogercresseyi) resistance in Atlantic salmon (Salmo salar). Genet Sel Evol 49:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gjedrem T, Rye M (2018) Selection response in fish and shellfish: a review. Rev Aquac 10:168–179

    Article  Google Scholar 

  • Gonzalez-Pena D, Gao G, Baranski M, Moen T, Cleveland BM, Kenney PB, Vallejo RL, Palti Y, Leeds TD (2016) Genome-wide association study for identifying loci that affect fillet yield, carcass, and body weight traits in rainbow trout (Oncorhynchus mykiss). Front Genet 7:203

    Article  PubMed  PubMed Central  Google Scholar 

  • Gutierrez AP, Yáñez JM, Fukui S, Swift B, Davidson WS (2015) Genome-wide association study (GWAS) for growth rate and age at sexual maturation in Atlantic salmon (Salmo salar). PLoS One 10:e0119730

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gutierrez AP, Yáñez JM, Davidson WS (2016) Evidence of recent signatures of selection during domestication in an Atlantic salmon population. Mar Genomics 26:41–50

    Article  CAS  PubMed  Google Scholar 

  • Houston RD, Haley CS, Hamilton A et al (2008) Major quantitative trait loci affect resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar). 1115:1109–1115

  • Houston RD, Taggart JB, Cézard T et al (2014) Development and validation of a high density SNP genotyping array for Atlantic salmon (Salmo salar). BMC Genomics 15:90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joshi R, Árnyasi M, Lien S et al (2018) Development and validation of 58K SNP-array and high-density linkage map in Nile tilapia (O. niloticus). Front Genet 9:472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li N, Zhou T, Geng X, Jin Y, Wang X, Liu S, Xu X, Gao D, Li Q, Liu Z (2018) Identification of novel genes significantly affecting growth in catfish through GWAS analysis. Mol Gen Genomics 293:587–599

    Article  CAS  Google Scholar 

  • Lien S, Koop BF, Sandve SR et al (2016) The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Sun L, Li Y, Sun F, Jiang Y, Zhang Y, Zhang J, Feng J, Kaltenboeck L, Kucuktas H, Liu Z (2014) Development of the catfish 250K SNP array for genome-wide association studies. BMC Res Notes 7:135

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Liu S, Yao J et al (2016) The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat Commun 7

  • López ME, Benestan L, Moore J, Perrier C, Gilbey J, di Genova A, Maass A, Diaz D, Lhorente JP, Correa K, Neira R, Bernatchez L, Yáñez JM (2019a) Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins. Evol Appl 12:137–156

    Article  PubMed  Google Scholar 

  • Lopez MED, Linderoth T, Norris A et al (2019b) Multiple selection signatures in farmed Atlantic salmon adapted to different environments across Hemispheres. Front Genet 10:901

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moen T, Baranski M, Sonesson AK, Kjøglum S (2009) Confirmation and fine-mapping of a major QTL for resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar): population-level associations between markers and trait. BMC Genomics 10:368

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neira R (2010) Breeding in aquaculture species: genetic improvement programs in developing countries. In: Proceedings of the 9th World Congress on Genetics Applied to Livestock Production, vol 8. Leipzig, Germany

  • Neira R, García X, Lhorente JP et al (2016) Evaluation of the growth and carcass quality of diallel crosses of four strains of Nile tilapia (Oerochromis niloticus). Aquaculture 451:213–222

    Article  Google Scholar 

  • Norris A (2017) Application of genomics in salmon aquaculture breeding programs by Ashie Norris: who knows where the genomic revolution will lead us? Mar Genomics 36:13–15

    Article  PubMed  Google Scholar 

  • Ødegård J, Moen T, Santi N et al (2014) Genomic prediction in an admixed population of Atlantic salmon (Salmo salar). Front Genet 5:1–8

    Google Scholar 

  • Palaiokostas C, Ferarreso S, Franch R, et al (2016) Genomic prediction of resistance to pasteurellosis in gilthead sea bream (Sparus aurata) using 2b-RAD sequencing. G3 (Bethesda) X:1–8

  • Palti Y, Gao G, Liu S et al (2015) The development and characterization of a 57K single nucleotide polymorphism array for rainbow trout. Mol Ecol Resour 15:662–672

    Article  CAS  PubMed  Google Scholar 

  • Ponzoni RW, Nguyen NH, Khaw HL et al (2011) Genetic improvement of Nile tilapia (Oreochromis niloticus) with special reference to the work conducted by the WorldFish Center with the GIFT strain. Rev Aquac 3:27–41

    Article  Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reis Neto RV, Yoshida GM, Lhorente JP, Yáñez JM (2019) Genome-wide association analysis for body weight identifies candidate genes related to development and metabolism in rainbow trout (Oncorhynchus mykiss). Mol Genet Genomics 294:563–571

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez FH, Flores-Mara R, Yoshida GM et al (2019) Genome-wide association analysis for resistance to infectious pancreatic necrosis virus identifies candidate genes involved in viral replication and immune response in rainbow trout (Oncorhynchus mykiss). G3 (Bethesda). https://doi.org/10.1534/g3.119.400463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sae-Lim P, Kause A, Lillehammer M, Mulder HA (2017) Estimation of breeding values for uniformity of growth in Atlantic salmon (Salmo salar) using pedigree relationships or single-step genomic evaluation. Genet Sel Evol 49:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsai HY, Hamilton A, Tinch AE et al (2015) Genome wide association and genomic prediction for growth traits in juvenile farmed Atlantic salmon using a high density SNP array. BMC Genomics 16:1–9

    Article  CAS  Google Scholar 

  • Vallejo RL, Leeds TD, Fragomeni BO et al (2016) Evaluation of genome-enabled selection for bacterial cold water disease resistance using progeny performance data in rainbow trout: insights on genotyping methods and genomic prediction models. Front Genet 7:1–13

    Article  CAS  Google Scholar 

  • Vallejo R, Liu S, Gao G et al (2017) Similar genetic architecture with shared and unique quantitative trait loci for bacterial cold water disease resistance in two rainbow trout breeding populations. Front Genet 8:1–15

    Article  CAS  Google Scholar 

  • Vallejo RL, Silva RMO, Evenhuis JP et al (2018) Accurate genomic predictions for BCWD resistance in rainbow trout are achieved using low-density SNP panels: evidence that long-range LD is a major contributing factor. J Anim Breed Genet 135:263–274

    Article  CAS  Google Scholar 

  • Webster C, Lim C (2006) Tilapia: biology, culture, and nutrition

  • Yáñez JM, Martinez V (2010) Genetic factors involved in resistance to infectious diseases in salmonids and their application in breeding programmes. Arch Med Vet 42:1–13

    Article  Google Scholar 

  • Yáñez JM, Houston RD, Newman S (2014) Genetics and genomics of disease resistance in salmonid species. Front Genet 5:1–13

    Google Scholar 

  • Yáñez JM, Newman S, Houston RD (2015) Genomics in aquaculture to better understand species biology and accelerate genetic progress. Front Genet 6:1–3

    Google Scholar 

  • Yañez JM, Naswa S, Lopez ME et al (2016) Genomewide single nucleotide polymorphism discovery in Atlantic salmon (Salmo salar): validation in wild and farmed American and European populations. Mol Ecol Resour 16:1002–1011

    Article  PubMed  CAS  Google Scholar 

  • Yáñez JM, Yoshida GM, Parra Á, Correa K, Barría A, Bassini LN, Christensen KA, López ME, Carvalheiro R, Lhorente JP, Pulgar R (2019) Comparative genomic analysis of three salmonid species identifies functional candidate genes involved in resistance to the intracellular bacterium Piscirickettsia salmonis. Front Genet 10:665

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshida GM, Lhorente JP, Carvalheiro R, Yáñez JM (2017) Bayesian genome-wide association analysis for body weight in farmed Atlantic salmon (Salmo salar L.). Anim Genet 48:698–703

    Article  CAS  PubMed  Google Scholar 

  • Yoshida G, Bangera R, Carvalheiro R et al (2018a) Genomic prediction accuracy for resistance against Piscirickettsia salmonis in farmed rainbow trout. G3 (Bethesda) 8:719–726

    Article  Google Scholar 

  • Yoshida G, Carvalheiro R, Rodríguez FH, Lhorente JP (2018b) Genomics single-step genomic evaluation improves accuracy of breeding value predictions for resistance to infectious pancreatic necrosis virus in rainbow trout. Genomics 111:127–132

    Article  CAS  PubMed  Google Scholar 

  • Yoshida GM, Barria A, Cáceres G et al (2019a) Genome-wide patterns of population structure and linkage disequilibrium in farmed Nile tilapia (Oreochromis niloticus). Front Genet 10:745

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshida GM, Lhorente JP, Correa K et al (2019b) Genome-wide association study and cost-efficient genomic predictions for growth and fillet yield in Nile tilapia (Oreochromis niloticus). G3 (Bethesda) 9

  • Zeng Q, Fu Q, Li Y et al (2017) Development of a 690 K SNP array in catfish and its application for genetic mapping and validation of the reference genome sequence. Sci Rep 7:1–14

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the Aqua America and Aquacorporación Internacional for kindly providing the samples used in this work, and Gabriel Rizzato and Natalí Kunita from Aqua America and Diego Salas and José Soto from Aquacorporación International for their contribution of the samples from Brazil and Costa Rica, respectively.

Funding

This study was partially funded from CORFO grant number 14EIAT-28667 from the Government of Chile. This work was supported by the Basal grant of the Center for Mathematical Modeling AFB170001 (UMI2807 UCHILE-CNRS) and the Center for Genome Regulation Fondap Grant 15090007 Powered@NLHPC. This research was partially supported by the supercomputing infrastructure of the NLHPC (ECM-02).

Author information

Author notes

  1. Agustín Barria

    Present address: The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK

  2. María E. López

    Present address: Department of Animal Breeding and Genetics, Swedish University of Agricultural Sciences, Uppsala, Sweden

Authors and Affiliations

  1. Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santiago, Chile

    José M. Yáñez, Grazyella Yoshida, Agustín Barria, Giovanna Cáceres, María I. Cádiz, María E. López & Ana Jedlicki

  2. Núcleo Milenio INVASAL, Concepción, Chile

    José M. Yáñez

  3. Benchmark Genetics Chile, Puerto Montt, Chile

    Grazyella Yoshida & Jean P. Lhorente

  4. Centro para la Regulación del Genoma, Universidad de Chile, Santiago, Chile

    Ricardo Palma-Véjares, Dante Travisany, Diego Díaz & Alejandro Maass

  5. Centro de Modelamiento Matemático UMI CNRS 2807, Universidad de Chile, Santiago, Chile

    Ricardo Palma-Véjares, Dante Travisany, Diego Díaz & Alejandro Maass

  6. Grupo Acuacorporacion, Internacional (GACI), Cañas, Costa Rica

    José Soto & Diego Salas

Authors
  1. José M. Yáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Grazyella Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agustín Barria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo Palma-Véjares
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dante Travisany
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Diego Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giovanna Cáceres
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. María I. Cádiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. María E. López
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jean P. Lhorente
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ana Jedlicki
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. José Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Diego Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Alejandro Maass
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.M.Y. conceived of and designed the study, contributed to the analysis, and drafted the manuscript. G.Y. contributed to the analysis and writing. A.B. drafted the first version of the manuscript. G.C., M.E.L., and A.J. participated in the data collection, purification, and management of the samples for sequencing and genotyping. R.P., D.D., D.T., and A.M. assisted with the bioinformatics analysi and contributed to writing. J.P.L. participated in the design of the study and writing. JS and DS contributed to the collection of the samples and managmenent of populations from Costa Rica. All authors have reviewed and approved the manuscript.

Corresponding author

Correspondence to José M. Yáñez.

Ethics declarations

Conflict of Interest

Two commercial organizations (Aquainnovo and Illumina) were involved in the SNP identification and preparation of the manuscript. GMY and JPL were employed by Benchmark Genetics Chile during the course of the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yáñez, J.M., Yoshida, G., Barria, A. et al. High-Throughput Single Nucleotide Polymorphism (SNP) Discovery and Validation Through Whole-Genome Resequencing in Nile Tilapia (Oreochromis niloticus). Mar Biotechnol 22, 109–117 (2020). https://doi.org/10.1007/s10126-019-09935-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09935-5

Keywords

Search

Navigation