Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits
Abstract Background Selective breeding is a promising solution to reduce the vulnerability of fish farms to heat waves, which are predicted to increase in intensity and frequency. However, limited information about the genetic architecture of acute hyperthermia resistance in fish is available. Two b...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | deu |
| Published: |
BMC
2023-06-01
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| Series: | Genetics Selection Evolution |
| Online Access: | https://doi.org/10.1186/s12711-023-00811-4 |
| _version_ | 1797801672035008512 |
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| author | Henri Lagarde Delphine Lallias Pierre Patrice Audrey Dehaullon Martin Prchal Yoannah François Jonathan D’Ambrosio Emilien Segret Ana Acin-Perez Frederic Cachelou Pierrick Haffray Mathilde Dupont-Nivet Florence Phocas |
| author_facet | Henri Lagarde Delphine Lallias Pierre Patrice Audrey Dehaullon Martin Prchal Yoannah François Jonathan D’Ambrosio Emilien Segret Ana Acin-Perez Frederic Cachelou Pierrick Haffray Mathilde Dupont-Nivet Florence Phocas |
| author_sort | Henri Lagarde |
| collection | DOAJ |
| description | Abstract Background Selective breeding is a promising solution to reduce the vulnerability of fish farms to heat waves, which are predicted to increase in intensity and frequency. However, limited information about the genetic architecture of acute hyperthermia resistance in fish is available. Two batches of sibs from a rainbow trout commercial line were produced: the first (N = 1382) was phenotyped for acute hyperthermia resistance at nine months of age and the second (N = 1506) was phenotyped for main production traits (growth, body length, muscle fat content and carcass yield) at 20 months of age. Fish were genotyped on a 57 K single nucleotide polymorphism (SNP) array and their genotypes were imputed to high-density based on the parent’s genotypes from a 665 K SNP array. Results The heritability estimate of resistance to acute hyperthermia was 0.29 ± 0.05, confirming the potential of selective breeding for this trait. Since genetic correlations of acute hyperthermia resistance with the main production traits near harvest age were all close to zero, selecting for acute hyperthermia resistance should not impact the main production traits, and vice-versa. A genome-wide association study revealed that resistance to acute hyperthermia is a highly polygenic trait, with six quantitative trait loci (QTL) detected, but explaining less than 5% of the genetic variance. Two of these QTL, including the most significant one, may explain differences in acute hyperthermia resistance across INRAE isogenic lines of rainbow trout. Differences in mean acute hyperthermia resistance phenotypes between homozygotes at the most significant SNP was 69% of the phenotypic standard deviation, showing promising potential for marker-assisted selection. We identified 89 candidate genes within the QTL regions, among which the most convincing functional candidates are dnajc7, hsp70b, nkiras2, cdk12, phb, fkbp10, ddx5, cygb1, enpp7, pdhx and acly. Conclusions This study provides valuable insight into the genetic architecture of acute hyperthermia resistance in juvenile rainbow trout. We show that the selection potential for this trait is substantial and selection for this trait should not be too detrimental to improvement of other traits of interest. Identified functional candidate genes provide new knowledge on the physiological mechanisms involved in acute hyperthermia resistance, such as protein chaperoning, oxidative stress response, homeostasis maintenance and cell survival. |
| first_indexed | 2024-03-13T04:54:02Z |
| format | Article |
| id | doaj.art-e30acdf23b7741fcadbaf4c97c4d5ac1 |
| institution | Directory Open Access Journal |
| issn | 1297-9686 |
| language | deu |
| last_indexed | 2024-03-13T04:54:02Z |
| publishDate | 2023-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Genetics Selection Evolution |
| spelling | doaj.art-e30acdf23b7741fcadbaf4c97c4d5ac12023-06-18T11:03:51ZdeuBMCGenetics Selection Evolution1297-96862023-06-0155112110.1186/s12711-023-00811-4Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traitsHenri Lagarde0Delphine Lallias1Pierre Patrice2Audrey Dehaullon3Martin Prchal4Yoannah François5Jonathan D’Ambrosio6Emilien Segret7Ana Acin-Perez8Frederic Cachelou9Pierrick Haffray10Mathilde Dupont-Nivet11Florence Phocas12Université Paris-Saclay, INRAE, AgroParisTech, GABIUniversité Paris-Saclay, INRAE, AgroParisTech, GABISYSAAF, French Poultry, Aquaculture and Insect Breeders AssociationUniversité Paris-Saclay, INRAE, AgroParisTech, GABIFaculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in České BudějoviceSYSAAF, French Poultry, Aquaculture and Insect Breeders AssociationSYSAAF, French Poultry, Aquaculture and Insect Breeders AssociationViviers de SarranceViviers de SarranceViviers de SarranceSYSAAF, French Poultry, Aquaculture and Insect Breeders AssociationUniversité Paris-Saclay, INRAE, AgroParisTech, GABIUniversité Paris-Saclay, INRAE, AgroParisTech, GABIAbstract Background Selective breeding is a promising solution to reduce the vulnerability of fish farms to heat waves, which are predicted to increase in intensity and frequency. However, limited information about the genetic architecture of acute hyperthermia resistance in fish is available. Two batches of sibs from a rainbow trout commercial line were produced: the first (N = 1382) was phenotyped for acute hyperthermia resistance at nine months of age and the second (N = 1506) was phenotyped for main production traits (growth, body length, muscle fat content and carcass yield) at 20 months of age. Fish were genotyped on a 57 K single nucleotide polymorphism (SNP) array and their genotypes were imputed to high-density based on the parent’s genotypes from a 665 K SNP array. Results The heritability estimate of resistance to acute hyperthermia was 0.29 ± 0.05, confirming the potential of selective breeding for this trait. Since genetic correlations of acute hyperthermia resistance with the main production traits near harvest age were all close to zero, selecting for acute hyperthermia resistance should not impact the main production traits, and vice-versa. A genome-wide association study revealed that resistance to acute hyperthermia is a highly polygenic trait, with six quantitative trait loci (QTL) detected, but explaining less than 5% of the genetic variance. Two of these QTL, including the most significant one, may explain differences in acute hyperthermia resistance across INRAE isogenic lines of rainbow trout. Differences in mean acute hyperthermia resistance phenotypes between homozygotes at the most significant SNP was 69% of the phenotypic standard deviation, showing promising potential for marker-assisted selection. We identified 89 candidate genes within the QTL regions, among which the most convincing functional candidates are dnajc7, hsp70b, nkiras2, cdk12, phb, fkbp10, ddx5, cygb1, enpp7, pdhx and acly. Conclusions This study provides valuable insight into the genetic architecture of acute hyperthermia resistance in juvenile rainbow trout. We show that the selection potential for this trait is substantial and selection for this trait should not be too detrimental to improvement of other traits of interest. Identified functional candidate genes provide new knowledge on the physiological mechanisms involved in acute hyperthermia resistance, such as protein chaperoning, oxidative stress response, homeostasis maintenance and cell survival.https://doi.org/10.1186/s12711-023-00811-4 |
| spellingShingle | Henri Lagarde Delphine Lallias Pierre Patrice Audrey Dehaullon Martin Prchal Yoannah François Jonathan D’Ambrosio Emilien Segret Ana Acin-Perez Frederic Cachelou Pierrick Haffray Mathilde Dupont-Nivet Florence Phocas Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits Genetics Selection Evolution |
| title | Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits |
| title_full | Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits |
| title_fullStr | Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits |
| title_full_unstemmed | Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits |
| title_short | Genetic architecture of acute hyperthermia resistance in juvenile rainbow trout (Oncorhynchus mykiss) and genetic correlations with production traits |
| title_sort | genetic architecture of acute hyperthermia resistance in juvenile rainbow trout oncorhynchus mykiss and genetic correlations with production traits |
| url | https://doi.org/10.1186/s12711-023-00811-4 |
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