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

Abstract

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.

Adipose tissue mitochondrial respiration in Atlantic salmon: implications for sex-dependent life-history variation

“…Such inherent high coupling capacity of salmon with the late maturation genotype may indicate that they could be more vulnerable to low food conditions such as during winters in freshwater (52) or in the sea (53). In line with this, a lower aerobic scope at the whole animal level –indicating lower capacity for aerobic metabolism beyond self-maintenance– in juvenile salmon with the late maturation genotype was also found by Prokkola et al (19). Further, the lower coupling capacity of the late maturation genotype matches the distribution of salmon with contrasting age-at-maturity in the wild, where individuals maturing later spawn typically in larger rivers that are likely more environmentally stable.…”

“…Finally, vgll3 early maturation genotype is linked to higher body condition in salmon (20). Therefore, adipose tissue processes could provide a functional basis of variation in age-at-maturity, and subsequently, potential evolutionary constraints (15, 19).…”

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

“…Given this, the lack of difference in SMR prior to maturation or prior to a change in body condition does not support SMR of juvenile salmon as a mediator of vgll3 effects on age at maturity at this particular age and in these conditions. Finally, these results were supported by a parallel study using a different crossing design and juvenile salmon of larger body size (Prokkola et al, 2021) where no association between SMR and vgll3 genotype was found.…”

“…We initially planned to also measure metabolic rate under exhaustive swimming to obtain data on maximum metabolic rate (MMR), but had to abandon these trials as we were unable to motivate juvenile salmon of this age and size to do any exhaustive swimming, either by swim tunnel or by hand chasing. This behavior might be specific to this life stage, as we were eventually successfully able to exercise fish up to MMR by hand chasing in a parallel study using a cohort from the same year that was studied 1–2 summer months later when the fish had grown from 1 to 4 g (Prokkola et al, 2021). Besides supporting our finding on the lack of an association between SMR and vgll3 genotype, Prokkola et al (2021) found a significantly higher MMR and aerobic scope in vgll3*EE compared to vgll3 *LL individuals, indicating that vgll3 genotype does affect the metabolic phenotype, but does so by affecting traits related to MMR without affecting SMR.…”

“…This behavior might be specific to this life stage, as we were eventually successfully able to exercise fish up to MMR by hand chasing in a parallel study using a cohort from the same year that was studied 1–2 summer months later when the fish had grown from 1 to 4 g (Prokkola et al, 2021). Besides supporting our finding on the lack of an association between SMR and vgll3 genotype, Prokkola et al (2021) found a significantly higher MMR and aerobic scope in vgll3*EE compared to vgll3 *LL individuals, indicating that vgll3 genotype does affect the metabolic phenotype, but does so by affecting traits related to MMR without affecting SMR. In the wild, juvenile Atlantic salmon prefer staying in slow‐velocity microhabitats where they act as sit‐and‐wait predators, darting out to catch suitable prey items as they pass by (Fraser et al, 1993; Metcalfe et al, 1997).…”