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.
Highlights
Physiological processes control how life-history diversity emerges from resource allocation and acquisition trade-offs [1]
Vgll3 genotype interacted with six6, such that maximum metabolic rate (MMR) was decreased when late maturation genotypes of the two loci cooccurred compared to other genotype combinations
In line with our hypothesis, we found that the vgll3 early maturation genotype increased the aerobic scope (AS) of juvenile Atlantic salmon compared to the late maturation genotype
Summary
Physiological processes control how life-history diversity emerges from resource allocation and acquisition trade-offs [1]. The rate of aerobic energy metabolism is a pivotal mechanism contributing to life-history variation—it modulates resource acquisition, provides cells with ATP, and constrains energy allocation to different body components and functions. Theories such as the metabolic theory of ecology and the pace-of-life syndrome theory [2,3] suggest metabolic rate covaries with life-history variation within and among species. This covariation may have a genetic basis, constraining trait evolution [4], yet only a few studies have demonstrated intraspecific genetic covariation or coevolution between metabolic rate and life-history traits [5,6,7]. High aerobic performance comes with costs, including maintaining a larger heart and gill surface area (associated with increased demand for osmoregulation) [12,16,17]
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