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.

FishResp is a user-friendly tool for calculating oxygen uptake of aquatic organisms. The aim of the software is to improve the quality of metabolic rate estimates based on a straightforward pipeline: background respiration correction, detection of mechanical problems, conduction of QC tests, and filtration based on user-defined criteria.

Metabolic rate is considered to determine the energetic investment placed into life-history traits, regulating the speed of an organism’s life-cycle and forming the so called “pace-of-life”. However, how metabolic rate and life-history traits co-evolve remains unclear. For instance, the energetic demands of life-history traits, including the number of energy allocation trade-offs, is unlikely to remain constant over ontogeny. Therefore, the predicted coevolution between metabolic rate and life-history could be specific to particular ontogenetic stages, rather than a stable property of an organism. Here, we test the ontogenetic dependency of the coevolution between metabolic rate and the pace of life-history, under strictly standardized conditions using 30 species of killifish, which are either annual species adapted to ephemeral pools or non-annual species inhabiting more permanent waterbodies. Standard metabolic rates were estimated at three ontogenetic stages, together with relevant life-history traits, i.e. growth (juveniles), maturity (young adults), and reproductive rate (reproductive adults). Life-history traits largely followed predicted pace-of-life patterns, with overall faster/higher rates in annual species. The divergences in life-history traits across species tended to increase over ontogeny, being smallest during juvenile growth and largest in reproductive adults. However, associations between life-history strategy and metabolic rate followed a reversed pattern, being strongest in juveniles, but lowest in reproductive adults. Our results are concordant with the number of energetic trade-offs increasing over ontogeny, which results in a stronger covariation between physiology and life-history traits earlier in ontogeny.

Conspecifics inhabiting divergent environments frequently differ in morphology, physiology, and performance, but the interrelationships amongst traits and with Darwinian fitness remains poorly understood. We investigated population differentiation in morphology, metabolic rate, and swimming performance in three‐spined sticklebacks (Gasterosteus aculeatus L.), contrasting a marine/ancestral population with two distinct freshwater morphotypes derived from it: the “typical” low‐plated morph, and a unique “small‐plated” morph. We test the hypothesis that similar to plate loss in other freshwater populations, reduction in lateral plate size also evolved in response to selection. Additionally, we test how morphology, physiology, and performance have evolved in concert as a response to differences in selection between marine and freshwater environments. We raised pure‐bred second‐generation fish originating from three populations and quantified their lateral plate coverage, burst‐ and critical swimming speeds, as well as standard and active metabolic rates. Using a multivariate Q ST‐F ST framework, we detected signals of directional selection on metabolic physiology and lateral plate coverage, notably demonstrating that selection is responsible for the reduction in lateral plate coverage in a small‐plated stickleback population. We also uncovered signals of multivariate selection amongst all bivariate trait combinations except the two metrics of swimming performance. Divergence between the freshwater and marine populations exceeded neutral expectation in morphology and in most physiological and performance traits, indicating that adaptation to freshwater habitats has occurred, but through different combinations of traits in different populations. These results highlight both the complex interplay between morphology, physiology and performance in local adaptation, and a framework for their investigation.

1. The physiological underpinnings of life history adaptations in ectotherms are not well understood. Theories suggest energy metabolism influences life history variation via modulation of resource acquisition. However, the genetic basis of this relation and its dependence on ecological conditions, such as food availability, have rarely been characterized, despite being critical to predicting the responses of populations to environmental changes. 2. The Atlantic salmon (Salmo salar) is an emerging wild model species for addressing these questions; strong genetic determination of age-at-maturity at two unlinked genomic regions (vgll3 and six6) enables the use of complex experimental designs and tests of hypotheses on the physiological and genetic basis of life-history trait variation. 3. In this study, we crossed salmon to obtain individuals with all combinations of late and early maturation genotypes for vgll3 and six6 within full-sib families. Using more than 250 juveniles in common garden conditions, we tested (i) whether metabolic phenotypes (i.e., standard and maximum metabolic rates, and absolute aerobic scope) were correlated with the age-at-maturity genotypes and (ii) if high vs. low food availability modulated the relationship. 4. We found that salmon with vgll3 early maturation genotype had a higher aerobic scope and maximum metabolic rate, but not standard metabolic rate, compared to salmon with vgll3 late maturation genotype. This suggests that physiological or structural pathways regulating maximum oxygen supply or demand are potentially important for the determination of age-at-maturity in Atlantic salmon. 5. Vgll3 and six6 exhibited physiological epistasis, whereby maximum metabolic rate significantly decreased when late maturation genotypes were present concurrently in both loci compared to other genotype combinations. 6. The growth of the feed restricted group decreased substantially compared to the high food group. However, the effects of life-history genomic regions were similar in both feeding regimes, indicating a lack of genotype-by-environment interactions. 7. Our results indicate that aerobic performance of juvenile salmon may affect their age-at-maturity. The results may help to better understand the mechanistic basis of life-history variation, and the metabolic constrains on life-history evolution.