QTLs Associated with Resistance to Cardiomyopathy Syndrome in Atlantic Salmon

Abstract

Cardiomyopathy syndrome (CMS) caused by piscine myocarditis virus is a major disease affecting the Norwegian Atlantic salmon industry. Three different populations of Atlantic salmon from the Mowi breeding program were used in this study. The first 2 populations (population 1 and 2) were naturally infected in a field outbreak, while the third population (population 3) went through a controlled challenged test. The aim of the study was to estimate the heritability, the genetic correlation between populations and perform genome-wide association analysis for resistance to this disease. Survival data from population 1 and 2 and heart atrium histology score data from population 3 was analyzed. A total of 571, 4312, and 901 fish from population 1, 2, and 3, respectively were genotyped with a noncommercial 55,735 Affymetrix marker panel. Genomic heritability ranged from 0.12 to 0.46 and the highest estimate was obtained from the challenge test dataset. The genetic correlation between populations was moderate (0.51-0.61). Two chromosomal regions (SSA27 and SSA12) contained single nucleotide polymorphisms associated with resistance to CMS. The highest association signal (P = 6.9751 × 10-27) was found on chromosome 27. Four genes with functional roles affecting viral resistance (magi1, pi4kb, bnip2, and ha1f) were found to map closely to the identified quantitative trait loci (QTLs). In conclusion, genetic variation for resistance to CMS was observed in all 3 populations. Two important quantitative trait loci were detected which together explain half of the total genetic variance, suggesting strong potential application for marker-assisted selection and genomic predictions to improve CMS resistance.

Keywords: Atlantic salmon; QTL analysis; cardiomyopathy syndrome; field outbreak; genetic correlations; heritability.

Figure 1.

Distribution of traits in the 3 population. (A) Binary phenotype (dead or survived) recorded in population 1, (B) binary phenotype (dead or survived) recorded in population 2, and (C) heart tissue (atrium) histology scores (0 to 3) recorded in population 3.

Figure 2.

Manhattan plot of resistance to cardiomyopathy syndrome (CMS). (A) Binary phenotype recorded from field outbreak on the commercial farm population 1. (B) Binary phenotype recorded from field outbreak of the informant pedigreed population 2. (C) Histology score of heart tissue (atrium) based on challenge test information of the informant pedigreed population 3. Red and blue horizontal line represent genome-wide significant threshold ($-lo{g}_{10}P=6.03$) and chromosomal-wide significant threshold for the population ($-lo{g}_{10}P=4.56$), respectively. See online version for full colors.

Figure 3.

Quantile–quantile plot of $-lo{g}_{10}P$ values for each of the 3 populations. See online version for full colors.

Figure 4.

Manhattan plots of chromosome 12 and 27 for the 3 populations; (a), (b), (c), and (d) are plots from population 1; (e) and (f) are plots from population 2; and (g), (h), (i), and (j) are plots from population 3. Plots (b), (d), (f), (h), and (j) were obtained by fitting the top most significant marker as covariate in the genome-wide association analysis. Red and blue horizontal line represent the genome-wide significant threshold ($-lo{g}_{10}P=6.03$) and the chromosomal-wide significant threshold for the population ($-lo{g}_{10}P=4.56$), respectively. See online version for full colors.