Circadian rhythms and environmental disturbances–underexplored interactions

Biological rhythms control the life of virtually all organisms, impacting numerous aspects ranging from subcellular processes to behaviour. Many studies have shown that changes in abiotic environmental conditions can disturb or entrain circadian (∼24 h) rhythms. These expected changes are so large that they could impose risks to the long-term viability of populations. Climate change is a major global stressor affecting the fitness of animals, partially because it challenges the adaptive associations between endogenous clocks and temperature – consequently, one can posit that a large-scale natural experiment on the plasticity of rhythm–temperature interactions is underway. Further risks are posed by chemical pollution and the depletion of oxygen levels in aquatic environments. Here, we focused our attention on fish, which are at heightened risk of being affected by human influence and are adapted to diverse environments showing predictable changes in light conditions, oxygen saturation and temperature. The examined literature to date suggests an abundance of mechanisms that can lead to interactions between responses to hypoxia, pollutants or pathogens and regulation of endogenous rhythms, but also reveals gaps in our understanding of the plasticity of endogenous rhythms in fish and in how these interactions may be disturbed by human influence and affect natural populations. Here, we summarize research on the molecular mechanisms behind environment–clock interactions as they relate to oxygen variability, temperature and responses to pollutants, and propose ways to address these interactions more conclusively in future studies.</p

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 Atlantic 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.Peer reviewe

Postrelease exploration and diel activity of hatchery, wild, and hybrid strain brown trout in seminatural streams

Behaviour that is adaptive in captivity may be maladaptive in the wild and compromise postrelease survival of hatchery fish. The understanding of behavioural variation displayed immediately after release could help to improve hatchery protocols and development of behavioural tests for assessing the fitness of fish reared for releases. We characterized the postrelease behaviour of common-garden-raised offspring of wild resident, captive-bred migratory, and hybrid brown trout (Salmo trutta) in two experiments: in small artificial channels and in high and low densities in seminatural streams. The results from seminatural streams showed that hatchery fish were more likely to disperse downstream from the initial stocking site compared with hybrid and wild strain fish. The small-scale experiment did not reveal this ecologically pivotal difference in postrelease performance among strains, and individual responses were inconsistent between the experiments. Circadian activity patterns did not differ among strains. These detailed observations of postrelease behaviour reveal important intrinsic differences in dispersal traits among brown trout strains and suggest that selective breeding and crossbreeding can substantially affect these traits.Peer reviewe

Sex-Specific Co-expression Networks and Sex-Biased Gene Expression in the Salmonid Brook Charr <i>Salvelinus fontinalis</i>.

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 salmonid Brook Charr Salvelinus fontinalis to characterize sex-specific co-expression networks in the liver of 47 female and 53 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, revealing 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

Different relationship between hsp70 mRNA and hsp70 levels in the heat shock response of two salmonids with dissimilar temperature preference

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Different relationship between hsp70 mRNA and hsp70 levels in the heat shock response of two salmonids with dissimilar temperature preference

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Fishing-induced versus natural selection in different brown trout (Salmo trutta) strains

Wild, adfluvial brown trout (Salmo trutta) are iconic targets in recreational fisheries but also endangered in many native locations. We compared how fishing and natural selection affect the fitness-proxies of brown trout from two pure angling-selected strains and experimental crosses between an adfluvial, hatchery-bred strain and three wild, resident strains. We exposed age 1+ parr to predation risk under controlled conditions where their behaviour was monitored with PIT-telemetry, and stocked age 2+ fish in two natural lakes for experimental fishing. Predation mortality (16% of the fish) was negatively size-dependent, while capture probability, also reflecting survival, in the lakes (38.9% of the fish) was positively length- and condition- dependent. Angling-induced selection against low boldness and slow growth rates relative to gillnet fishing indicated gear-dependent potential for fisheries-induced evolution in behaviours and life-histories. Offspring of wild, resident fish showed slower growth rates than the crossbred strains. Strain effects suggested significant heritable scope for artificial selection on life-history traits and demonstrated that choices of fish supplementation by stocking may override the genetic effects induced by angling.Peer reviewe

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.Peer reviewe

Comparing RADseq and microsatellites for estimating genetic diversity and relatedness - Implications for brown trout conservation

The conservation and management of endangered species requires information on their genetic diversity, relatedness and population structure. The main genetic markers applied for these questions are microsatellites and single nucleotide polymorphisms (SNPs), the latter of which remain the more resource demanding approach in most cases. Here, we compare the performance of two approaches, SNPs obtained by restriction-site-associated DNA sequencing (RADseq) and 16 DNA microsatellite loci, for estimating genetic diversity, relatedness and genetic differentiation of three, small, geographically close wild brown trout (Salmo trutta) populations and a regionally used hatchery strain. The genetic differentiation, quantified as F-ST, was similar when measured using 16 microsatellites and 4,876 SNPs. Based on both marker types, each brown trout population represented a distinct gene pool with a low level of interbreeding. Analysis of SNPs identified half- and full-siblings with a higher probability than the analysis based on microsatellites, and SNPs outperformed microsatellites in estimating individual-level multilocus heterozygosity. Overall, the results indicated that moderately polymorphic microsatellites and SNPs from RADseq agreed on estimates of population genetic structure in moderately diverged, small populations, but RADseq outperformed microsatellites for applications that required individual-level genotype information, such as quantifying relatedness and individual-level heterozygosity. The results can be applied to other small populations with low or moderate levels of genetic diversity.Peer reviewe