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Variation in volatile organic compounds in Atlantic salmon mucus is associated with resistance to salmon lice infection.

ABSTRACT: Salmon lice are ectoparasites that threaten wild and farmed salmonids. Artificial selection of salmon for resistance to the infectious copepodid lice stage currently relies on in vivo challenge trials on thousands of salmon a year. We challenged 5750 salmon with salmon lice (Lepeophtheirus salmonis) from two distinct farmed strains of salmon in two separate trials. We found that volatile organic compounds (VOC), 1-penten-3-ol, 1-octen-3-ol and 6-methyl-5-hepten-2-one in the mucus of the salmon host after salmon lice infection, were significantly associated with lice infection numbers across a range of water temperatures (5 °C, 10 °C, 17 °C). Some VOCs (benzene, 1-octen-3-ol and 3,5,5-trimethyl-2-hexene) were significantly different between lines divergently selected for salmon lice resistance. In a combined population assessment, selected VOCs varied between families in the range of 47- 59% indicating a genetic component and were positively correlated to the salmon hosts estimated breeding values 0.59-0.74. Mucosal VOC phenotypes could supplement current breeding practices and have the potential to be a more direct and ethical proxy for salmon lice resistance provided they can be measured prior to lice infestation.

SUBMITTER: Difford GF

PROVIDER: S-EPMC8940922 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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Variation in volatile organic compounds in Atlantic salmon mucus is associated with resistance to salmon lice infection.

Difford G F GF Haugen J-E JE Aslam M L ML Johansen L H LH Breiland M W MW Hillestad B B Baranski M M Boison S S Moghadam H H Jacq C C

Scientific reports 20220322 1

Salmon lice are ectoparasites that threaten wild and farmed salmonids. Artificial selection of salmon for resistance to the infectious copepodid lice stage currently relies on in vivo challenge trials on thousands of salmon a year. We challenged 5750 salmon with salmon lice (Lepeophtheirus salmonis) from two distinct farmed strains of salmon in two separate trials. We found that volatile organic compounds (VOC), 1-penten-3-ol, 1-octen-3-ol and 6-methyl-5-hepten-2-one in the mucus of the salmon h ...[more]

PMID: 35318390

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Project description:BackgroundSea lice have significant negative economic and welfare impacts on marine Atlantic salmon farming. Since host resistance to sea lice has a substantial genetic component, selective breeding can contribute to control of lice. Genomic selection uses genome-wide marker information to predict breeding values, and can achieve markedly higher accuracy than pedigree-based methods. Our aim was to assess the genetic architecture of host resistance to sea lice, and test the utility of genomic prediction of breeding values. Individual lice counts were measured in challenge experiments using two large Atlantic salmon post-smolt populations from a commercial breeding programme, which had genotypes for ~33 K single nucleotide polymorphisms (SNPs). The specific objectives were to: (i) estimate the heritability of host resistance; (ii) assess its genetic architecture by performing a genome-wide association study (GWAS); (iii) assess the accuracy of predicted breeding values using varying SNP densities (0.5 to 33 K) and compare it to that of pedigree-based prediction; and (iv) evaluate the accuracy of prediction in closely and distantly related animals.ResultsHeritability of host resistance was significant (0.22 to 0.33) in both populations using either pedigree or genomic relationship matrices. The GWAS suggested that lice resistance is a polygenic trait, and no genome-wide significant quantitative trait loci were identified. Based on cross-validation analysis, genomic predictions were more accurate than pedigree-based predictions for both populations. Although prediction accuracies were highest when closely-related animals were used in the training and validation sets, the benefit of having genomic-versus pedigree-based predictions within a population increased as the relationships between training and validation sets decreased. Prediction accuracy reached an asymptote with a SNP density of ~5 K within populations, although higher SNP density was advantageous for cross-population prediction.ConclusionsHost resistance to sea lice in farmed Atlantic salmon has a significant genetic component. Phenotypes relating to host resistance can be predicted with moderate to high accuracy within populations, with a major advantage of genomic over pedigree-based methods, even at relatively sparse SNP densities. Prediction accuracies across populations were low, but improved with higher marker densities. Genomic selection can contribute to lice control in salmon farming.

Project description:Sea lice (Caligus rogercresseyi) are ectoparasitic copepods which have a large negative economic and welfare impact in Atlantic salmon (Salmo salar) aquaculture, particularly in Chile. A multi-faceted prevention and control strategy is required to tackle lice, and selective breeding contributes via cumulative improvement of host resistance to the parasite. While host resistance has been shown to be heritable, little is yet known about the individual loci that contribute to this resistance, the potential underlying genes, and their mechanisms of action. In this study we took a multifaceted approach to identify and characterize quantitative trait loci (QTL) affecting host resistance in a population of 2,688 Caligus-challenged Atlantic salmon post-smolts from a commercial breeding program. We used low and medium density genotyping with imputation to collect genome-wide SNP marker data for all animals. Moderate heritability estimates of 0.28 and 0.24 were obtained for lice density (as a measure of host resistance) and growth during infestation, respectively. Three QTL explaining between 7 and 13% of the genetic variation in resistance to sea lice (as represented by the traits of lice density) were detected on chromosomes 3, 18, and 21. Characterisation of these QTL regions was undertaken using RNA sequencing and pooled whole genome sequencing data. This resulted in the identification of a shortlist of potential underlying causative genes, and candidate functional mutations for further study. For example, candidates within the chromosome 3 QTL include a putative premature stop mutation in TOB1 (an anti-proliferative transcription factor involved in T cell regulation) and an uncharacterized protein which showed significant differential allelic expression (implying the existence of a cis-acting regulatory mutation). While host resistance to sea lice is polygenic in nature, the results of this study highlight significant QTL regions together explaining between 7 and 13 % of the heritability of the trait. Future investigation of these QTL may enable improved knowledge of the functional mechanisms of host resistance to sea lice, and incorporation of functional variants to improve genomic selection accuracy.

Project description:Sea lice (Caligus rogercresseyi) is an ectoparasite which causes major production losses in the salmon aquaculture industry worldwide. Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) are two of the most susceptible salmonid species to sea lice infestation. The objectives of this study were to: (1) identify genomic regions associated with resistance to Caligus rogercresseyi in Atlantic salmon and rainbow trout by performing single-step Genome-Wide Association studies (ssGWAS), and (2) identify candidate genes related to trait variation based on exploring orthologous genes within the associated regions across species. A total of 2626 Atlantic salmon and 2643 rainbow trout were challenged and genotyped with 50 K and 57 K SNP panels, respectively. We ran two independent ssGWAS for sea lice resistance on each species and identified 7 and 13 regions explaining more than 1% of the genetic variance for the trait, with the most important regions explaining 3% and 2.7% for Atlantic salmon and rainbow trout, respectively. We identified genes associated with immune response, cytoskeleton function, and cell migration when focusing on important genomic regions for each species. Moreover, we found 15 common orthogroups which were present in more than one associated genomic region, within- or between-species; however, only one orthogroup showed a clear potential biological relevance in the response against sea lice. For instance, dual-specificity protein phosphatase 10-like (dusp10) and dual-specificity protein phosphatase 8 (dusp8) were found in genomic regions associated with lice density in Atlantic salmon and rainbow trout, respectively. Dusp10 and dusp8 are modulators of the MAPK pathway and might be involved in the differences of the inflammation response between lice resistant and susceptible fish from both species. Our results provide further knowledge on candidate genes related to sea lice resistance and may help establish better control for sea lice in fish populations.

Dataset Information

Variation in volatile organic compounds in Atlantic salmon mucus is associated with resistance to salmon lice infection.

Publications

Variation in volatile organic compounds in Atlantic salmon mucus is associated with resistance to salmon lice infection.

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