Genome-wide association analysis of the resistance to infectious hematopoietic necrosis virus in two aquaculture rainbow trout strains confirms oligogenic architecture with several moderate effect quantitative trait loci

Authors: Palti, Yniv; Vallejo, Roger; PURCELL, MAUREEN - Us Geological Survey (USGS); Gao, Guangtu; Shewbridge, Kristy; Long, Roseanna; SETZKE, CHRISTOPHER - University Of Washington; FRAGOMENI, BRENO - University Of Connecticut; CHENG, HAO - University Of California; MARTIN, KYLE - Troutlodge, Inc; NAISH, KERRY - University Of Washington

Submitted to: Frontiers in Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/30/2024
Publication Date: 5/24/2024
Citation: Palti, Y., Vallejo, R.L., Purcell, M., Gao, G., Shewbridge, K., Long, R., Setzke, C., Fragomeni, B., Cheng, H., Martin, K., Naish, K. 2024. Genome-wide association analysis of the resistance to infectious hematopoietic necrosis virus in two aquaculture rainbow trout strains confirms oligogenic architecture with several moderate effect quantitative trait loci. Frontiers in Genetics. 15:1394656. https://doi.org/10.3389/fgene.2024.1394656.
DOI: https://doi.org/10.3389/fgene.2024.1394656

Interpretive Summary: Infectious hematopoietic necrosis (IHN) is a disease of salmonid fish that is caused by the IHN virus (IHNV). Under intensive aquaculture conditions, IHNV can cause significant mortality and economic losses. Currently, there is no proven and cost-effective method for IHNV control. Using genome-enabled approaches for selective breeding for traits that cannot be measured directly in the potential breeders, like disease resistance, holds a great promise as it provides individual genetic merit estimate for potential breeders compared to family-average estimates in traditional selective breeding. In aquaculture, it has been shown that genomic approaches can rapidly enhance genetic improvements for traits that are controlled by a few genes with large effect on the phenotype. Previously we found that genetic resistance to IHNV is controlled by the oligogenic inheritance of several moderate effect quantitative trait loci (QTL) and many small effect loci in a commercial rainbow trout breeding population that has been under selection pressure for the trait. In the current study, we used genome wide association analyses in two different commercial aquaculture strains that were naïve to previous exposure to IHNV with the assumption that we are more likely to find large effect QTL in populations that have not been previously selected for resistance to IHNV disease. However, this assumption was found to be incorrect as no major QTL with large effect were identified in the two populations. At the same time, similarly to the previous study, moderate heritability was estimated to the trait, indicating that selective breeding can be used to improve the genetic basis for resistance to IHNV disease in the commercial populations of rainbow trout that are widely used by the aquaculture industry. In addition, several of the moderate-effect QTL were shared by the two populations and were found to contain candidate genes that may be involved in the rainbow trout antiviral response. Further research on the association of those genome loci with disease resistance and how the genes that they harbor may be involved in the fish antiviral response will help improving our understanding of the biological basis of resistance to IHNV in rainbow trout.

Technical Abstract: Infectious hematopoietic necrosis (IHN) is a disease of salmonid fish that is caused by the IHN virus (IHNV), which can cause significant mortality and economic losses in rainbow trout aquaculture and fisheries enhancement hatchery programs. In a previous study, we found that genetic resistance to IHNV is controlled by the oligogenic inheritance of several moderate effect quantitative trait loci (QTL) and many small effect loci in a commercial rainbow trout breeding population that has been under selection pressure for the trait. Here we used genome wide association analyses in two different commercial aquaculture strains that were naïve to previous exposure to IHNV. However, no major QTL were detected despite the naïve status of the two strains in the current study, and our analyses confirmed an oligogenic architecture for genetic resistance to IHNV in rainbow trout. A total of 1,859 and 1,768 offspring from two commercial aquaculture strains were phenotyped for resistance to IHNV and genotyped with the rainbow trout Axiom 57K SNP array. Moderate heritability values (0.15 - 0.25) were estimated. Two statistical methods were used for genome wide association analyses in the two populations. Overall, 17 QTL with notable effect (AGV=1.9%) were detected in at least one of the two rainbow trout strains with at least one of the two statistical methods. Six of those QTL were mapped to the same chromosomal regions in both strains, and two were previously mapped to overlapping chromosomal regions in the third aquaculture strain of rainbow trout from our previous study. Although none of the loci was detected with large enough effect to merit marker assisted selection without further evaluation and validation, we conclude that some of the loci merit further investigation to better understand the biological basis of IHN disease resistance across populations.