Standard metabolic rate does not associate with age‐at‐maturity genotype in juvenile Atlantic salmon

Åsheim, Eirik Ryvoll; Prokkola, Jenni M.; Morozov, Sergey; Aykanat, Tutku; Primmer, Craig R.

doi:10.1002/ece3.8408

Cited by 8 publications

(8 citation statements)

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“…It can also be relevant to survival of salmon after spawning, and thereby repeated spawning (iteroparity), which is co-inherited with the same vgll3 genotype as early maturation [ 101 ]. However, the lack of sex differences in metabolic phenotypes in our study both across and within age-at-maturity genotypes, suggests that sex-dependent life-history variation in salmon [ 33 ] is not reflected in metabolic rates during the juvenile stage (see also [ 91 ]).…”

Section: Discussionmentioning

confidence: 87%

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Genetic coupling of life-history and aerobic performance in Atlantic salmon

et al. 2022

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A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions ( vgll3 and six6 ) makes Atlantic salmon ( Salmo salar ) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes—standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS)—and the life-history genomic regions, and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Furthermore, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve.

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Section: Discussionmentioning

confidence: 87%

“…1 g) compared to this study (mean approx. 4 g) [ 91 ]. The lack of association to the age-at-maturity loci is unexpected, as SMR, or basal metabolic rate in endotherms, has been proposed to explain life-history variation along the fast-slow axis [ 5 , 7 ], but see [ 92 ].…”

Section: Discussionmentioning

confidence: 99%

Genetic coupling of life-history and aerobic performance in Atlantic salmon

et al. 2022

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“…In addition, fish fed the S0.15 diet showed a reduction in standard metabolic energy. Standard metabolic energy refers to energy expenditure for organ maintenance, nutrient assimilation, and adaptation to changes in resource availability ( 74 ). In free-living pike ( Esox lucius ), standard metabolic energy comprises up to 90% of the energy budget ( 75 ).…”

Section: Discussionmentioning

confidence: 99%

Dietary Succinate Impacts the Nutritional Metabolism, Protein Succinylation and Gut Microbiota of Zebrafish

Ding

Hao

et al. 2022

Front. Nutr.

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Succinate is widely used in the food and feed industry as an acidulant, flavoring additive, and antimicrobial agent. This study investigated the effects of dietary succinate on growth, energy budget, nutritional metabolism, protein succinylation, and gut microbiota composition of zebrafish. Zebrafish were fed a control-check (0% succinate) or four succinate-supplemented diets (0.05, 0.10, 0.15, and 0.2%) for 4 weeks. The results showed that dietary succinate at the 0.15% additive amount (S0.15) can optimally promote weight gain and feed intake. Whole body protein, fat, and energy deposition increased in the S0.15 group. Fasting plasma glucose level decreased in fish fed the S0.15 diet, along with improved glucose tolerance. Lipid synthesis in the intestine, liver, and muscle increased with S0.15 feeding. Diet with 0.15% succinate inhibited intestinal gluconeogenesis but promoted hepatic gluconeogenesis. Glycogen synthesis increased in the liver and muscle of S0.15-fed fish. Glycolysis was increased in the muscle of S0.15-fed fish. In addition, 0.15% succinate-supplemented diet inhibited protein degradation in the intestine, liver, and muscle. Interestingly, different protein succinylation patterns in the intestine and liver were observed in fish fed the S0.15 diet. Intestinal proteins with increased succinylation levels were enriched in the tricarboxylic acid cycle while proteins with decreased succinylation levels were enriched in pathways related to fatty acid and amino acid degradation. Hepatic proteins with increased succinylation levels were enriched in oxidative phosphorylation while proteins with decreased succinylation levels were enriched in the processes of protein processing and transport in the endoplasmic reticulum. Finally, fish fed the S0.15 diet had a higher abundance of Proteobacteria but a lower abundance of Fusobacteria and Cetobacterium. In conclusion, dietary succinate could promote growth and feed intake, promote lipid anabolism, improve glucose homeostasis, and spare protein. The effects of succinate on nutritional metabolism are associated with alterations in the levels of metabolic intermediates, transcriptional regulation, and protein succinylation levels. However, hepatic fat accumulation and gut microbiota dysbiosis induced by dietary succinate suggest potential risks of succinate application as a feed additive for fish. This study would be beneficial in understanding the application of succinate as an aquatic feed additive.

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“…anaerobic capacity) in the intestine of, for example, fish with six6 LL - vgll3 EE genotype, could improve fish growth [50] or the ability for osmoregulation when entering the marine environment [51], if the difference is consistent in salmon at sea. However, if variation in vgll3 and six6 shapes the function of tissues via CS and LDH content, it appears to not affect SMR [38,39], thus suggesting a mechanism that is not related to maintaining growth potential. Previously, digestion and feeding have been linked to ecotype differences in salmonids; in rainbow trout ( Oncorhynchus mykiss ), fast-growing piscivorous ecotypes maintain an active digestive tract and higher assimilation efficiency than slow-growing insectivorous ecotypes [85].…”

Section: Discussionmentioning

confidence: 99%

“…5% of variation in MMR; in juvenile salmon, individuals that carry homozygous late-maturation genotypes in both loci (i.e. vgll3 LL and six6 LL ) have a lower MMR compared to the additive expectations of both genotypes [38], but there is no difference in SMR between the early and late maturation genotypes [38,39]. Based on their expression patterns, v gll3 and six6 may exert their effects on phenotypes, for example via cell fate commitment [40,41], but it is not known which mechanisms induce the effects on MMR, or if the loci exert other tissue-specific effects on metabolism that could influence the timing of maturation.…”

Section: Introductionmentioning

confidence: 99%

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

Prokkola,

Chew,

Anttila

et al. 2024

Phil. Trans. R. Soc. B

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Metabolic rates, including standard (SMR) and maximum (MMR) metabolic rate have often been linked with life-history strategies. Variation in context- and tissue-level metabolism underlying SMR and MMR may thus provide a physiological basis for life-history variation. This raises a hypothesis that tissue-specific metabolism covaries with whole-animal metabolic rates and is genetically linked to life history. In Atlantic salmon ( Salmo salar ), variation in two loci, vgll3 and six6 , affects life history via age-at-maturity as well as MMR. Here, using individuals with known SMR and MMR with different vgll3 and six6 genotype combinations, we measured proxies of mitochondrial density and anaerobic metabolism, i.e. maximal activities of the mitochondrial citrate synthase (CS) and lactate dehydrogenase (LDH) enzymes, in four tissues (heart, intestine, liver, white muscle) across low- and high-food regimes. We found enzymatic activities were related to metabolic rates, mainly SMR, in the intestine and heart. Individual loci were not associated with the enzymatic activities, but we found epistatic effects and genotype-by-environment interactions in CS activity in the heart and epistasis in LDH activity in the intestine. These effects suggest that mitochondrial density and anaerobic capacity in the heart and intestine may partly mediate variation in metabolic rates and life history via age-at-maturity. This article is part of the theme issue ‘The evolutionary significance of variation in metabolic rates’.

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Standard metabolic rate does not associate with age‐at‐maturity genotype in juvenile Atlantic salmon

Cited by 8 publications

References 85 publications

Genetic coupling of life-history and aerobic performance in Atlantic salmon

Genetic coupling of life-history and aerobic performance in Atlantic salmon

Dietary Succinate Impacts the Nutritional Metabolism, Protein Succinylation and Gut Microbiota of Zebrafish

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

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