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Prokkola, J. M.

Publications and source records attributed to Prokkola, J. M..

10 recordsLinked to original sources

The influence of parental and genotype effects on early survival and development in Atlantic salmon

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.

evolutionary biology↗

Aerobic scope is sustained through a heatwave in juvenile Atlantic salmon

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{degrees}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 {degrees}C before and after the heatwave, and after 4-5 days exposure at 19 and 22{degrees}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 SummaryIn 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.

physiology↗

Density-dependent expression of epitranscriptomic, stress, and appetite regulating genes in Atlantic salmon

Intraspecific competition due to e.g., 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 naturally occurring 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 m6A RNA methylation. This gene set includes paralog pairs, to account for potential functional divergence associated with salmonid genome duplication. 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 m6A 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 emphasize the value of integrating different physiological responses at the molecular level to better understand ecological processes affected by environmental change.

molecular biology↗

Food quality and vgll3 genotype influence reproductive traits in female Atlantic salmon

Age at maturity is an important factor contributing to life-history diversity. In Atlantic salmon, this trait often shows sex-specific variation, but female salmon are seldom included in experimental studies of maturation. As a result, there is a gap in our knowledge of how different genetic and environmental factors affect female maturation. Using a 4-year common-garden experiment, we assessed the influence of diet (low-fat vs. control) and vgll3 (a candidate gene in a genomic region known to influence age at maturity in Atlantic salmon) on maturation and related phenotypic traits of female Atlantic salmon from two 2nd-generation hatchery populations. We found the early-maturation-associated vgll3*E allele to be associated with higher probability of maturation. Heritability of maturation was estimated to be 0.295 with vgll3s contribution to phenotypic variance being [~]2%. In addition, both body size and body condition measured in the spring prior to spawning influenced maturation. Body condition, in turn, was influenced by population and diet. The northern Oulu population and the low-fat diet were associated with lower body condition compared to the 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 maturation and demonstrate that genes and environment interact to shape age at maturity in female Atlantic salmon.

evolutionary biology↗

Early survival in Atlantic salmon is associated with parental genotype at loci linked to timing of maturation late in life

Large effects loci often contain genes with critical developmental functions with potentially broad effects across life-stages. However, the 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 behavioural 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-nutrient, but not in 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 by 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.

evolutionary biology↗

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

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.

physiology↗

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

Atlantic salmon (Salmo salar) is a species with diverse life-history strategies, to which the timing of maturation contributes considerably. Recently, the genome region including the gene vgll3 has gained attention as a locus with a large effect on salmon maturation timing, and recent studies on the vgll3 locus in salmon have indicated that its effect might be mediated through body condition and accumulation of adipose tissue. However, the cellular and physiological pathways leading from vgll3 genotype to phenotype are still unknown. Standard metabolic rate is a potentially important trait for resource acquisition and assimilation and we hypothesized that this trait, being a proxy for the maintenance energy expenditure of an individual, could be an important link in the pathway from vgll3 genotype to maturation-timing phenotype. As a first step to studying links between vgll3 and the metabolic phenotype of Atlantic salmon, we measured the standard metabolic rate of 150 first year Atlantic salmon juveniles of both sexes, originating from 14 different families with either late maturing or early maturing vgll3 genotypes. No significant difference in mass-adjusted standard metabolic rate was detected between individuals with different vgll3 genotypes, indicating that juvenile salmon of different vgll3 genotypes have similar maintenance energy requirements in the experimental conditions used and that the effects of vgll3 on body condition and maturation are not strongly related to maintenance energy expenditure in either sex at this life stage. Summary statementWe show that vgll3, a gene known to have significant effects on Atlantic salmon (Salmo salar) life-history strategy, does not associate with standard metabolic rate in salmon juveniles.

genetics↗

Genetic coupling of life-history and aerobic performance in juvenile 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. Further, 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.

evolutionary biology↗

Behavioural and metabolic consequences after a single generation of angling selection in brown trout

The behavior of organisms can be subject to human induced selection such as that arising from fishing. Angling is expected to induce mortality on fish with bold and explorative behavior, which are behaviors commonly linked to a high standard metabolic rate. We studied the transgenerational response of brown trout (Salmo trutta) to angling-induced selection by examining the behavior and metabolism of 1-year-old parr between parents that were or were not captured by experimental fly fishing. We performed the angling selection experiment on both a wild and a captive population, and compared the offspring for standard metabolic rate and behavior under predation risk in common garden conditions. Angling had population-specific effects on risk taking and exploration tendency, but no effects on standard metabolic rate. Our study adds to the evidence that angling can induce transgenerational responses on fish personality. However, understanding the mechanisms of divergent responses between the populations requires further study on the selectivity of angling in various conditions.

animal behavior and cognition↗

Sex-specific and conserved gene co-expression networks underlie phenotypes within the paleopolyploid Salvelinus genus (Family Salmonidae)

Networks of co-expressed genes produce complex phenotypes associated with functional novelty. Sex differences in gene expression levels or in the structure of gene co-expression networks can cause sexual dimorphism and may resolve sexually antagonistic selection. Here we used RNA-sequencing in the paleopolyploid salmonid Brook Charr Salvelinus fontinalis to characterize sex-specific co-expression networks in the liver of 35 female and 51 male offspring. In both networks, modules were characterized for functional enrichment, hub gene identification, and associations with 15 growth, reproduction, and stress-related phenotypes. Modules were then evaluated for preservation in the opposite sex, and in the congener Arctic Charr Salvelinus alpinus. Overall, more transcripts were assigned to a module in the female network than in the male network, which coincided with higher inter-individual gene expression and phenotype variation in the females. Most modules were preserved between sexes and species, including those involved in conserved cellular processes (e.g. translation, immune pathways). However, two sex-specific male modules were identified, and these may contribute to sexual dimorphism. To compare with the network analysis, differentially expressed transcripts were identified between the sexes, finding a total of 16% of expressed transcripts as sex-biased. For both sexes, there was no overrepresentation of sex-biased genes or sex-specific modules on the putative sex chromosome. Sex-biased transcripts were also not overrepresented in sex-specific modules, and in fact highly male-biased transcripts were enriched in preserved modules. Comparative network analysis and differential expression analyses identified different aspects of sex differences in gene expression, and both provided new insights on the genes underlying sexual dimorphism in the salmonid Brook Charr.

genomics↗