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Associations between metabolic traits and growth rate in brown trout (Salmo trutta) depend on thermal regime.

ABSTRACT: Metabolism defines the energetic cost of life, yet we still know relatively little about why intraspecific variation in metabolic rate arises and persists. Spatio-temporal variation in selection potentially maintains differences, but relationships between metabolic traits (standard metabolic rate (SMR), maximum metabolic rate (MMR), and aerobic scope) and fitness across contexts are unresolved. We show that associations between SMR, MMR, and growth rate (a key fitness-related trait) vary depending on the thermal regime (a potential selective agent) in offspring of wild-sampled brown trout from two populations reared for approximately 15 months in either a cool or warm (+1.8°C) regime. SMR was positively related to growth in the cool, but negatively related in the warm regime. The opposite patterns were found for MMR and growth associations (positive in warm, negative in the cool regime). Mean SMR, but not MMR, was lower in warm regimes within both populations (i.e. basal metabolic costs were reduced at higher temperatures), consistent with an adaptive acclimation response that optimizes growth. Metabolic phenotypes thus exhibited a thermally sensitive metabolic 'floor' and a less flexible metabolic 'ceiling'. Our findings suggest a role for growth-related fluctuating selection in shaping patterns of metabolic variation that is likely important in adapting to climate change.

SUBMITTER: Archer LC

PROVIDER: S-EPMC8441116 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Metapopulation dynamics over the course of an invasion are usually difficult to grasp because they require large and reliable data collection, often unavailable. The invasion of the fish-free freshwater ecosystems of the remote sub-Antarctic Kerguelen Islands following man-made introductions of brown trout (Salmo trutta) in the 1950's is an exception to this rule. Benefiting from a full long term environmental research monitoring of the invasion, we built a Bayesian dynamic metapopulation model to analyze the invasion dynamics of 85 river systems over 51 years. The model accounted for patch size (river length and connections to lakes), alternative dispersal pathways between rivers, temporal trends in dynamics, and uncertainty in colonization date. The results show that the model correctly represents the observed pattern of invasion, especially if we assume a coastal dispersal pathway between patches. Landscape attributes such as patch size influenced the colonization function, but had no effect on propagule pressure. Independently from patch size and distance between patches, propagule pressure and colonization function were not constant through time. Propagule pressure increased over the course of colonization, whereas the colonization function decreased, conditional on propagule pressure. The resulting pattern of this antagonistic interplay is an initial rapid invasion phase followed by a strong decrease in the invasion rate. These temporal trends may be due to either adaptive processes or environmental gradients encountered along the colonization front. It was not possible to distinguish these two hypotheses. Because invasibility of Kerguelen Is. freshwater ecosystems is very high due to the lack of a pre-existing fish fauna and minimal human interference, our estimates of invasion dynamics represent a blueprint for the potential of brown trout invasiveness in pristine environments. Our conclusions shed light on the future of polar regions where, because of climate change, fish-free ecosystems become increasingly accessible to invasion by fish species.

Project description:BACKGROUND:Tetracapsuloides bryosalmonae is a myxozoan parasite which causes economically important and emerging proliferative kidney disease (PKD) in salmonids. Brown trout, Salmo trutta is a native fish species of Europe, which acts as asymptomatic carriers for T. bryosalmonae. There is only limited information on the molecular mechanism involved in the kidney of brown trout during T. bryosalmonae development. We employed RNA sequencing (RNA-seq) to investigate the global transcriptome changes in the posterior kidney of brown trout during T. bryosalmonae development. METHODS:Brown trout were exposed to the spores of T. bryosalmonae and posterior kidneys were collected from both exposed and unexposed control fish. cDNA libraries were prepared from the posterior kidney and sequenced. Bioinformatics analysis was performed using standard pipeline of quality control, reference mapping, differential expression analysis, gene ontology, and pathway analysis. Quantitative real time PCR was performed to validate the transcriptional regulation of differentially expressed genes, and their correlation with RNA-seq data was statistically analyzed. RESULTS:Transcriptome analysis identified 1169 differentially expressed genes in the posterior kidney of brown trout, out of which 864 genes (74%) were upregulated and 305 genes (26%) were downregulated. The upregulated genes were associated with the regulation of immune system process, vesicle-mediated transport, leucocyte activation, and transport, whereas the downregulated genes were associated with endopeptidase regulatory activity, phosphatidylcholine biosynthetic process, connective tissue development, and collagen catabolic process. CONCLUSION:To our knowledge, this is the first RNA-seq based transcriptome study performed in the posterior kidney of brown trout during active T. bryosalmonae development. Most of the upregulated genes were associated with the immune system process, whereas the downregulated genes were associated with other metabolic functions. The findings of this study provide insights on the immune responses mounted by the brown trout on the developing parasite, and the host molecular machineries modulated by the parasite for its successful multiplication and release.

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Associations between metabolic traits and growth rate in brown trout (Salmo trutta) depend on thermal regime.

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