Jenni Maria Prokkola

Parental qualities can influence the development and fitness of their offspring via genetic and non-genetic effects. Although these effects are often linked to parental phenotypes, the effect of parental genetic variation linked with relevant phenotypes is less well understood. We performed full factorial crosses based on parental genotypes for an age-at-maturity-related gene, vgll3, to investigate how the parental genotypes influence Atlantic salmon ( Salmo salar ) offspring survival, growth, and development in their early life. Beyond the connection with age at maturity, the additional association between vgll3 and body condition in Atlantic salmon offers a potential pathway by which the maternal vgll3 genotype could influence offspring early life fitness. Combined with measurements of maternal phenotype and egg characteristics, the crossing design therefore allowed us to disentangle the maternal and paternal genetic and non-genetic contributions to variation in offspring survival and phenotypic traits. The phenotypic traits measured were hatching length and yolk sac area, growth, and yolk sac consumption and conversion efficiency. Parental vgll3 genotype did not influence the majority of our measured egg traits or alevin traits except for a genetic effect of paternal vgll3 genotype on offspring survival, whereby the paternal late maturation allele was associated with higher survival. Maternal effects were strongest for survival and for traits associated with hatching and weaker for alevin growth and yolk sac usage. Paternal effects on the measured alevin traits were negligible. The results from our study demonstrate that both maternal and paternal effects have the potential to influence offspring early life fitness traits.

Intraspecific competition due to for example, density, has substantial influence on fitness dynamics and life histories, but the underlying physiological mechanisms are often complex and the molecular basis unclear. Further, designing laboratory experiments to measure physiological responses that reflect natural conditions is challenging. Here, we reared Atlantic salmon juveniles in semi‐wild conditions in two densities to investigate the molecular mechanism of density‐related changes in the hypothalamus, a key brain region regulating stress and energy homeostasis. We measured density‐dependent changes in the expression of 12 genes involved in appetite and stress regulation and 16 genes involved in post‐transcriptional regulation of gene expression via m ⁶ A RNA methylation. We also quantified genotype‐environment interactions between density and two major life‐history loci, vgll3 and six6 . We found significant density‐related differences in the expression of genes coding for corticotropin‐releasing factors, appetite stimulators and inhibitors and m ⁶ A RNA methylation actors. Moreover, a paralogue of an appetite inhibitor showed a density‐dependent pattern that was the opposite of what was expected. Six6 locus was also associated with changes in the expression of epitranscriptomic markers, including two writers and one eraser. Our results highlight that individuals' response to density in natural conditions is shaped by a complex interplay between stress, appetite and epitranscriptomic pathways in the hypothalamus. In addition, the functional divergence of paralogs indicates a potential role of genome duplication shaping such a response. We emphasise the value of integrating different physiological responses at the molecular level to better understand ecological processes affected by environmental change.

Atlantic Salmon life-histories are shaped by interactions between environmental and genetic factors. The mitochondrial NADP-dependent malic enzyme ( me3 or mMEP-2), historically described as a polymorphic allozyme varying across populations, has been associated with age at maturity in wild populations. However, more recently, other loci ( vgll3 and six6) have also been shown to influence age at maturity, and studies disentangling their relative effects are lacking. This is especially important given that me3 and vgll3 are located on the same chromosome. Here, we used a common-garden experiment to investigate the impact of the me3 locus on male parr maturation probability in a Finnish population while accounting for variation at the vgll3 and six6 loci. Although we found linkage disequilibrium between the me3 and vgll3 loci, me3 remained moderately associated with maturation probability even when vgll3 genotype was accounted for. Together, these results support observations from wild populations of a genetic effect of me3 on maturation probability, but they also highlight the importance of considering both me3 and vgll3 when investigating the mechanism linking these loci to maturation.

Aquatic ectotherms are vulnerable to heatwave-induced physiological stress, which arises from increased energy demands and reduced dissolved oxygen content in warmer waters. Understanding thermal physiology is critical for predicting how commercially and ecologically important populations could be affected by the increasing risk of rising temperatures. Heatwave risk assessments often examine extremities of time scales: immediate impacts or long-term consequences. However, little is known about how consistently increasing mid-term thermal stress shapes aerobic performance in commercially important species such as Atlantic salmon ( Salmo salar ), which may face heat stress in rivers, especially at the juvenile life stage. By measuring how salmon juveniles manage their aerobic capacity at 16, 19 and 22°C using intermittent respirometry, we test if their thermal performance curve shows a decline at temperatures commonly occurring during heatwaves. Whole-animal metabolism was measured from control individuals kept at 16 °C before and after the heatwave, and after 4-5 days exposure at 19 and 22°C during the heatwave. We show that standard metabolic rate increases with temperature, but maximum metabolic rate and aerobic scope do not change between these temperatures. These findings suggest that juvenile Atlantic salmon may have limited capacity to increase aerobic performance during moderate heatwaves, leaving them vulnerable to cumulative effects of oxygen limitation to vital functions such as growth and stress responses. As climate change intensifies, incorporating thermal performance curves into conservation strategies can be utilized for predicting population resilience and informing effective management. Lay Summary: In juvenile Atlantic salmon, standard metabolic rate increases but there is no difference in maximum metabolic rate and aerobic scope with increasing temperatures. Considering the increased metabolic costs of activities at higher temperatures, our results show that juvenile salmon are vulnerable to deteriorating performance at temperatures commonly experienced in present-day heatwaves.

Age at maturity is an important life‐history trait, often showing sex‐specific variation, contributing to life‐history diversity in many species. Atlantic salmon ( Salmo salar ) are an excellent model system to investigate genetic and environmental factors affecting sex‐specific maturation, yet few laboratory studies have focused on females as they mature later than males, on average. Using a 4‐year common‐garden experiment of Atlantic salmon, we assessed the influence of diet (low‐fat vs. control) and vgll3 (a candidate gene influencing maturation age) on maturation and related phenotypic traits of female Atlantic salmon derived from two second‐generation hatchery populations. We found the early‐maturation associated E allele to be additively associated with a higher probability of maturation. Heritability of maturation was estimated to be 0.295, with vgll3's contribution to phenotypic variance being ~2%. In addition, body condition measured in the spring prior to spawning influenced maturation. Body condition, in turn, was influenced by population and diet. The more northern Oulu population and the low‐fat diet were associated with lower body condition compared to the more southern Neva population and the control diet. Moreover, there was an interaction between population and diet on body condition, suggesting that populations may respond differently to nutrient availability. These results broaden our understanding of the processes underlying sex‐ and population‐specific maturation and demonstrate that genes and environment influence age at maturity in a species that displays sex‐specific variation in maturation.

Large effect loci often contain genes with critical developmental functions and potentially broad effects across life stages. However, their life stage-specific fitness consequences are rarely explored. In Atlantic salmon, variation in two large-effect loci, six6 and vgll3, is linked to age at maturity and several physiological and behavioral traits in early life. By genotyping the progeny of wild Atlantic salmon that were planted into natural streams with nutrient manipulations, we tested if genetic variation in these loci is associated with survival in early life. We found that higher early-life survival was linked to the genotype associated with late maturation in the vgll3, but with early maturation in the six6 locus. These effects were significant in high nutrients but not in low-nutrient streams. The differences in early survival were not explained by additive genetic effects in the offspring generation but by maternal genotypes in the six6 locus and by both parents’ genotypes in the vgll3 locus. Our results suggest that indirect genetic effects of large-effect loci can be significant determinants of offspring fitness. This study demonstrates an intriguing case of how large-effect loci can exhibit complex fitness associations across life stages in the wild and indicates that predicting evolutionary dynamics is difficult.

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’.

Adipose tissue is essential for energy homeostasis, with mitochondria having a central role in its function. Mitochondria-mediated white adipose tissue dysfunction has been linked to several metabolic disorders in humans but surprisingly little is known about natural variation in mitochondrial function in wild animal populations, and its evolutionary significance. Early sexual maturation (low age-at-maturity) in Atlantic salmon ( Salmo salar ) is promoted by higher adiposity and has a strong genetic association with the vgll3 locus. This makes Atlantic salmon a convenient wild model to study the potential role of mitochondria-mediated adipose tissue processes in relation to the timing of maturation. Yet, mitochondrial respiration has not been measured in the adipose tissue in fish, and the lack of data is restricting the development of informed hypotheses. Here, using 13 Atlantic salmon individuals reared in common-garden conditions, we first verified the feasibility of measuring mitochondrial respiration in the adipose tissue. As expected, the respiration level was generally low, but nonetheless we successfully quantified its biological variation in the adipose tissue. Next, we analysed the potential association of mitochondrial respiration with mitochondrial DNA (mtDNA) content, adipocyte size, sex, and the vgll3 genotype. Despite low samples sizes, mitochondrial respiration, leak respiration, and coupling capacity (P/E ratio) were marginally significantly decreased in immature females carrying with the vgll3 early maturation compared to the alternative genotype. Based on these results, we suggested two new hypotheses on how the coupling capacity of oxidative phosphorylation could be linked with the timing of maturation via adiposity and pave the way to study the mechanistic relationships between life-history variation and mitochondrial bioenergetics in wild populations.

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 (vgll3andsix6) 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 invgll3was 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.