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

Abstract

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’.

Consequences of the cost of living: is variation in metabolic rate evolutionarily significant?

“…selection [28,29] and heritability [30,31]) in the context of metabolic rates. This approach has the potential to improve our understanding of variation in metabolism measured at the whole-animal level and at other levels covered in this issue, including tissue-specific [32,33], cellular [34] and subcellular [33] metabolic activity. Genomic advances have allowed for studies that pinpoint genes involved in producing metabolic rate variation, as highlighted by Prokkola et al [32].…”

“…This approach has the potential to improve our understanding of variation in metabolism measured at the whole-animal level and at other levels covered in this issue, including tissue-specific [32,33], cellular [34] and subcellular [33] metabolic activity. Genomic advances have allowed for studies that pinpoint genes involved in producing metabolic rate variation, as highlighted by Prokkola et al [32]. These studies all link metabolic rate variation with some aspect of individual physiological function, and therefore potentially fitness.…”

“…Genomic advances have allowed for studies that pinpoint genes involved in producing metabolic rate variation, as highlighted by Prokkola et al . [ 32 ]. These studies all link metabolic rate variation with some aspect of individual physiological function, and therefore potentially fitness.…”

Early survival in Atlantic salmon is associated with parental genotypes at loci linked to timing of maturation

“…In addition, the genetic variation in these loci is associated with metabolic phenotypes, whereby juvenile salmon with the vgll3 early genotype exhibit a higher maximum metabolic rate and aerobic scope, with the former trait also affected by six6 loci via epistasis (Prokkola et al 2022). These genomic regions also show physiological epistasis via the maximal activities of mitochondrial and anaerobic metabolic enzymes in the heart and intestine (Prokkola et al 2024). Variation in six6 , in turn, has been associated with stomach content volume during ocean feeding (Aykanat et al 2020).…”