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

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.

Linking vgll3 genotype and aggressive behaviour in juvenile Atlantic salmon (Salmo salar).

We tested the possibility that vgll3, a gene linked with maturation age in Atlantic salmon (Salmo salar), may be associated with behaviour by measuring aggressiveness and feeding activity in 380 juveniles with different vgll3 genotypes. Contrary to our prediction, individuals with the genotype associated with later maturation (vgll3*LL) were significantly more aggressive than individuals with the genotype associated with earlier maturation (vgll3*EE). Individuals with higher aggression were also significantly lighter in colour and had higher feeding activity. Although higher aggression was associated with higher feeding activity, there was no association between feeding activity and vgll3 genotype. Increased aggression of vgll3*LL individuals was independent of their sex and size, and genotypes did not differ in their condition factor. These results imply that aggressive behaviour may have an energetic cost impairing growth and condition, especially when food cannot be monopolized. This may have implications for individual fitness and aquaculture practices.

Sex-specific associations of the maturation locus vgll3 with exploratory behavior and boldness in Atlantic salmon juveniles.

Studies linking genetics, behavior and life history in any species are rare. In Atlantic salmon (Salmo salar), age at maturity is a key life-history trait and associates strongly with the vgll3 locus, whereby the vgll3*E allele is linked with younger age at maturity, and higher body condition than the vgll3*L allele. However, the relationship between this genetic variation and behaviors like boldness and exploration which may impact growth and reproductive strategies is poorly understood. The pace-of-life syndrome (POLS) framework provides predictions, whereby heightened exploratory behavior and boldness are predicted in individuals with the early maturation-associated vgll3 genotype (EE). Here, we tested these predictions by investigating the relationship between vgll3 genotypes and exploration and boldness behaviors in 129 juveniles using the novel environment and novel object trials. Our results indicated that contrary to POLS predictions, vgll3*LL fish were bolder and more explorative, suggesting a genotype-level syndrome including several behaviors. Interestingly, clear sex differences were observed in the latency to move in a new environment, with vgll3*EE males, but not females, taking longer to move than their vgll3*LL counterparts. Our results provide further empirical support for recent calls to consider more nuanced explanations than the pace of life theory for integrating behavior into life-history theory.