Genomic selection (GS) is increasingly applied in breeding programs of major aquaculture species, enabling improved prediction accuracy and genetic gain compared to pedigree-based approaches. Koi Herpesvirus disease (KHVD) is notifiable by the World Organization for Animal Health and the European Union, causing major economic losses to carp production. GS has potential to breed carp with improved resistance to KHVD, thereby contributing to disease control. In the current study, Restriction-site Associated DNA sequencing (RAD-seq) was applied on a population of 1,425 common carp juveniles which had been challenged with Koi herpes virus, followed by sampling of survivors and mortalities. GS was tested on a wide range of scenarios by varying both SNP densities and the genetic relationships between training and validation sets. The accuracy of correctly identifying KHVD resistant animals using GS was between 8 and 18% higher than pedigree best linear unbiased predictor (pBLUP) depending on the tested scenario. Furthermore, minor decreases in prediction accuracy were observed with decreased SNP density. However, the genetic relationship between the training and validation sets was a key factor in the efficacy of genomic prediction of KHVD resistance in carp, with substantially lower prediction accuracy when the relationships between the training and validation sets did not contain close relatives.

Department of Animal Breeding and Genetics Swedish University of Agricultural Sciences Uppsala Sweden

Faculty of Fisheries and Protection of Waters South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses University of South Bohemia České Budějovice Vodňany Czechia

Royal School of Veterinary Studies The Roslin Institute The University of Edinburgh Midlothian United Kingdom

Veterinary Research Institute Brno Czechia

Zobrazit více v PubMed

Aguilar I., Misztal I., Legarra A., Tsuruta S. (2011). Efficient computation of the genomic relationship matrix and other matrices used in single-step evaluation. J. Anim. Breed. Genet. 128 422–428. 10.1111/j.1439-0388.2010.00912.x PubMed DOI

Aslam M. L., Carraro R., Bestin A., Cariou S., Sonesson A. K., Haffray P., et al. (2018). Genetics of resistance to photobacteriosis in gilthead sea bream (Sparus aurata) using 2b-RAD sequencing. BMC Genet. 19:43. 10.1186/s12863-018-0631-x PubMed DOI PMC

Baird N. A., Etter P. D., Atwood T. S., Currey M. C., Shiver A. L., Lewis Z. A., et al. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376. 10.1371/journal.pone.0003376 PubMed DOI PMC

Barría A., Christensen K. A., Yoshida G. M., Correa K., Jedlicki A., Lhorente J. P., et al. (2018). Genomic predictions and genome-wide association study of resistance against piscirickettsia salmonis in coho salmon (Oncorhynchus kisutch) using ddRAD sequencing. G3 8 1183–1194. 10.1534/g3.118.200053 PubMed DOI PMC

Calus M. P. L., Vandenplas J. (2018). SNPrune: an efficient algorithm to prune large SNP array and sequence datasets based on high linkage disequilibrium. Genet. Sel. Evol. 50:34. 10.1186/s12711-018-0404-z PubMed DOI PMC

Catchen J. M., Amores A., Hohenlohe P., Cresko W., Postlethwait J. H. (2011). Stacks: building and genotyping Loci de novo from short-read sequences. G3 1 171–182. 10.1534/g3.111.000240 PubMed DOI PMC

Correa K., Bangera R., Figueroa R., Lhorente J. P., Yáñez J. M. (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. 10.1186/s12711-017-0291-8 PubMed DOI PMC

Dixon P. F., Joiner C. L., Way K., Reese R. A., Jeney G., Jeney Z., et al. (2009). Comparison of the resistance of selected families of common carp, Cyprinus carpio L., to koi herpesvirus: preliminary study. J. Fish Dis. 32 1035–1039. 10.1111/j.1365-2761.2009.01081.x PubMed DOI

Ferdosi M. H., Kinghorn B. P., van der Werf J. H. J., Lee S. H., Gondro C. (2014). hsphase: an R package for pedigree reconstruction, detection of recombination events, phasing and imputation of half-sib family groups. BMC Bioinformatics 15:172. 10.1186/1471-2105-15-172 PubMed DOI PMC

Gjedrem T., Rye M. (2016). Selection response in fish and shellfish: a review. Rev. Aquacult. 10 168–179. 10.1111/raq.12154 DOI

Habier D., Fernando R. L., Garrick D. J. (2013). Genomic BLUP decoded: a look into the black box of genomic prediction. Genetics 194 597–607. 10.1534/genetics.113.152207 PubMed DOI PMC

Habier D., Fernando R. L., Kizilkaya K., Garrick D. J. (2011). Extension of the bayesian alphabet for genomic selection. BMC Bioinformatics 12:186. 10.1186/1471-2105-12-186 PubMed DOI PMC

Hanley A. J., McNeil J. B. (1982). The meaning and use of the area under a receiver operating characteristic (ROC) Curve. Radiology 143 29–36. 10.1148/radiology.143.1.7063747 PubMed DOI

Henderson C. R. (1975). Best linear unbiased estimation and prediction under a selection model. Biometrics 31 423–447. PubMed

Hickey J. M., Chiurugwi T., Mackay I., Powell W. (2017). Genomic prediction unifies animal and plant breeding programs to form platforms for biological discovery. Nat. Genet. 49 1297–1303. 10.1038/ng.3920 PubMed DOI

Houston R. D., Brasileira R., De Zootecnia (2017). Invited review future directions in breeding for disease resistance in aquaculture species. Bras. Zootec. 46 545–551. 10.1590/s1806-92902017000600010 DOI

Houston R. D., Haley C. S., Hamilton A., Guy D. R., Tinch A. E., et al. (2008). Major quantitative trait loci affect resistance to infectious pancreatic necrosis in Atlantic salmon (Salmo salar). Genetics 178 1109–1115. 10.1534/genetics.107.082974 PubMed DOI PMC

Kizilkaya K., Fernando R. L., Garrick D. J. (2010). Genomic prediction of simulated multibreed and purebred performance using observed fifty thousand single nucleotide polymorphism genotypes. J. Anim. Sci. 88 544–551. 10.2527/jas.2009-2064 PubMed DOI

Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Legarra A., Christensen O. F., Aguilar I., Misztal I. (2014). Single Step, a general approach for genomic selection. Livest. Sci. 166 54–65. 10.1016/j.livsci.2014.04.029 DOI

Lillehammer M., Meuwissen T. H. E., Sonesson A. K. (2013). A low-marker density implementation of genomic selection in aquaculture using within-family genomic breeding values. Genet. Sel. Evol. 45:39. 10.1186/1297-9686-45-39 PubMed DOI PMC

Meuwissen T., Hayes B., Goddard M. (2013). Accelerating improvement of livestock with genomic selection. Annu. Rev. Anim. Biosci. 1 221–237. 10.1146/annurev-animal-031412-103705 PubMed DOI

Meuwissen T., Hayes B., Goddard M. (2016). Genomic selection: a paradigm shift in animal breeding. Anim. Front. 6 6–14. 10.2527/af.2016-0002 DOI

Meuwissen T. H. E., Hayes B. J., Goddard M. E. (2001). Prediction of total genetic value using genome-wide dense marker maps. Genetics 157 1819–1829. PubMed PMC

Moen T., Baranski M., Sonesson A. K., 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. 10.1186/1471-2164-10-368 PubMed DOI PMC

Ødegård J., Moen T., Santi N., Korsvoll S. A., Kjøglum S., Meuwissen T. H., et al. (2014). Genomic prediction in an admixed population of Atlantic salmon (Salmo salar). Front. Genet 5:402. 10.3389/fgene.2014.00402 PubMed DOI PMC

Ødegård J., Olesen I., Dixon P., Jeney Z., Nielsen H. M., Way K., et al. (2010). Genetic analysis of common carp (Cyprinus carpio) strains. II: resistance to koi herpesvirus and Aeromonas hydrophila and their relationship with pond survival. Aquaculture 304 7–13. 10.1016/j.aquaculture.2010.03.017 DOI

OIE (2018). OIE-Listed Diseases, Infections and Infestations in Force in 2018. Available at: http://www.oie.int/animal-health-in-the-world/oie-listed-diseases-2018/ (accessed March 26, 2018).

Palaiokostas C., Cariou S., Bestin A., Bruant J. S., Haffray P., Morin T., et al. (2018c). Genome-wide association and genomic prediction of resistance to viral nervous necrosis in European sea bass (Dicentrarchus labrax) using RAD sequencing. Genet. Sel. Evol. 50:30. 10.1186/s12711-018-0401-2 PubMed DOI PMC

Palaiokostas C., Kocour M., Prchal M., Houston R. D. (2018b). Accuracy of genomic evaluations of juvenile growth rate in common carp (Cyprinus carpio) using genotyping by sequencing. Front. Genet. 9:82. 10.3389/fgene.2018.00082 PubMed DOI PMC

Palaiokostas C., Robledo D., Vesely T., Prchal M., Pokorova D., Piackova V., et al. (2018a). Mapping and sequencing of a significant quantitative trait locus affecting resistance to koi herpesvirus in common carp. G3 8 3507–3513. 10.1534/g3.118.200593 PubMed DOI PMC

Pérez P., de los Campos G. (2014). Genome-wide regression and prediction with the BGLR statistical package. Genetics 198 483–495. 10.1534/genetics.114.164442 PubMed DOI PMC

Piačková V., Flajšhans M., Pokorová D., Reschová S., Gela D., Čížek A., et al. (2013). Sensitivity of common carp, Cyprinus carpio L., strains and crossbreeds reared in the Czech Republic to infection by cyprinid herpesvirus 3 (CyHV-3; KHV). J. Fish Dis. 36 75–80. 10.1111/jfd.12007 PubMed DOI

Plummer M., Best N., Cowles K., Vines K. (2006). CODA: convergence diagnosis and output analysis for MCMC. R News 6 7–11.

Pokorova D., Reschova S., Hulova J., Vicenova M., Vesely T., Piackova V. (2010). Detection of cyprinid herpesvirus-3 in field samples of common and koi carp by various single-round and nested PCR methods. J. World Aqua. Soc. 41 773–779. 10.1111/j.1749-7345.2010.00419.x DOI

Prchal M., Kause A., Vandeputte M., Gela D., Allamellou J.-M., et al. (2018a). The genetics of overwintering performance in two-year old common carp and its relation to performance until market size. PLoS One 13:e0191624. 10.1371/journal.pone.0191624 PubMed DOI PMC

Prchal M., Bugeon J., Vandeputte M., Kause A., Vergnet A., Zhao J., et al. (2018b). Potential for genetic improvement of the main slaughter yields in common carp with in vivo morphological predictors. Front. Genet. 9:283. 10.3389/fgene.2018.00283 PubMed DOI PMC

Robledo D., Matika O., Hamilton A., Houston R. D. (2018). Genome-wide association and genomic selection for resistance to amoebic gill disease in atlantic salmon. G3 8 1195–1203. 10.1534/g3.118.200075 PubMed DOI PMC

Robledo D., Palaiokostas C., Bargelloni L., Martínez P., Houston R. (2017). Applications of genotyping by sequencing in aquaculture breeding and genetics. Rev. Aquac. 10 670-682. PubMed PMC

Shapira Y., Magen Y., Zak T., Kotler M., Hulata G., Berta Levavi S. (2005). Differential resistance to koi herpes virus (KHV)/carp interstitial nephritis and gill necrosis virus (CNGV) among common carp (Cyprinus carpio L.) strains and crossbreds. Aquaculture 245 1–11. 10.1016/j.aquaculture.2004.11.038 DOI

Sonesson A. K., Meuwissen T. H. E. (2009). Testing strategies for genomic selection in aquaculture breeding programs. Genet. Sel. Evol. 41:37. 10.1186/1297-9686-41-37 PubMed DOI PMC

Tadmor-Levi R., Asoulin E., Hulata G., David L. (2017). Studying the genetics of resistance to CyHV-3 disease using introgression from feral to cultured common carp strains. Front. Genet. 8:24. 10.3389/fgene.2017.00024 PubMed DOI PMC

Taylor N. G. H., Dixon P. F., Jeffery K. R., Peeler E. J., Denham K. L., Way K., et al. (2010). Koi herpesvirus: distribution and prospects for control in England and Wales. J. Fish Dis. 33 221–230. 10.1111/j.1365-2761.2009.01111.x PubMed DOI

Tsai H.-Y., Hamilton A., Tinch A. E., Guy D. R., Bron J. E., Taggart J. B., et al. (2016). Genomic prediction of host resistance to sea lice in farmed Atlantic salmon populations. Genet. Sel. Evol. 48:47. 10.1186/s12711-016-0226-9 PubMed DOI PMC

Tsai H.-Y., Hamilton A., Tinch A. E., Guy D. R., Gharbi K., Stear M. J., 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 16:969. 10.1186/s12864-015-2117-9 PubMed DOI PMC

Tsairidou S., Woolliams J. A., Allen A. R., Skuce R. A., McBride S. H., Wright D. M., et al. (2014). Genomic prediction for tuberculosis resistance in dairy cattle. PLoS One 9:e96728. 10.1371/journal.pone.0096728 PubMed DOI PMC

Vallejo R. L., Leeds T. D., Fragomeni B. O., Gao G., Hernandez A. G., Misztal I., 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. 7:96. 10.3389/fgene.2016.00096 PubMed DOI PMC

Vallejo R. L., Liu S., Gao G., Fragomeni B. O., Hernandez A. G., Leeds T. D., 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. 8:156. 10.3389/fgene.2017.00156 PubMed DOI PMC

Vallejo R. L., Silva R. M. O., Evenhuis J. P., Gao G., Liu S., Parsons J. E., 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. 10.1111/jbg.12335 PubMed DOI

Vandeputte M., Kocour M., Mauger S., Dupont-Nivet M., De Guerry D., Gela D., et al. (2004). Heritability estimates for growth-related traits using microsatellite parentage assignment in juvenile common carp (Cyprinus carpio L.). Aquaculture 235 223–236. 10.1016/j.aquaculture.2003.12.019 DOI

Wray N. R., Yang J., Goddard M. E., Visscher P. M., Kimberly R. (2010). The genetic interpretation of area under the ROC curve in genomic profiling (Schork, N. J., Ed.). PLoS Genet. 6:e1000864. 10.1371/journal.pgen.1000864 PubMed DOI PMC

Xu P., Zhang X., Wang X., Li J., Liu G., Kuang Y., et al. (2014). Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat. Genet. 46 1212–1219. 10.1038/ng.3098 PubMed DOI

Yáñez J. M., Houston R. D., Newman S. (2014). Genetics and genomics of disease resistance in salmonid species. Front. Genet. 5:415 10.3389/fgene.2014.00415 PubMed DOI PMC

Yue G. H., Wang L. (2017). Current status of genome sequencing and its applications in aquaculture. Aquaculture 468 337–347. 10.3390/ijms19041083 PubMed DOI PMC