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Alternative migratory tactics in brown trout (Salmo trutta) are underpinned by divergent regulation of metabolic but not neurological genes.

ABSTRACT: The occurrence of alternative morphs within populations is common, but the underlying molecular mechanisms remain poorly understood. Many animals, for example, exhibit facultative migration, where two or more alternative migratory tactics (AMTs) coexist within populations. In certain salmonid species, some individuals remain in natal rivers all their lives, while others (in particular, females) migrate to sea for a period of marine growth. Here, we performed transcriptional profiling ("RNA-seq") of the brain and liver of male and female brown trout to understand the genes and processes that differentiate between migratory and residency morphs (AMT-associated genes) and how they may differ in expression between the sexes. We found tissue-specific differences with a greater number of genes expressed differentially in the liver (n = 867 genes) compared with the brain (n = 10) between the morphs. Genes with increased expression in resident livers were enriched for Gene Ontology terms associated with metabolic processes, highlighting key molecular-genetic pathways underlying the energetic requirements associated with divergent migratory tactics. In contrast, smolt-biased genes were enriched for biological processes such as response to cytokines, suggestive of possible immune function differences between smolts and residents. Finally, we identified evidence of sex-biased gene expression for AMT-associated genes in the liver (n = 12) but not the brain. Collectively, our results provide insights into tissue-specific gene expression underlying the production of alternative life histories within and between the sexes, and point toward a key role for metabolic processes in the liver in mediating divergent physiological trajectories of migrants versus residents.

SUBMITTER: Wynne R

PROVIDER: S-EPMC8216917 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:AbstractAnimals generally adjust their behavior in response to bodily state (e.g., size and energy reserves) to optimize energy intake in relation to mortality risk, weighing predation probability against the risk of starvation. Here, we investigated whether brown trout Salmo trutta adjust their behavior in relation to energetic status and body size during a major early-life selection bottleneck, when fast growth is important. Over two consecutive time periods (P1 and P2; 12 and 23 days, respectively), food availability was manipulated, using four different combinations of high (H) and low (L) rations (i.e., HH, HL, LH, and LL; first and second letter denoting ration during P1 and P2, respectively). Social effects were excluded through individual isolation. Following the treatment periods, fish in the HL treatment were on average 15-21 % more active than the other groups in a forced open-field test, but large within-treatment variation provided only weak statistical support for this effect. Furthermore, fish on L-ration during P2 tended to be more actively aggressive towards their mirror image than fish on H-ration. Body size was related to behavioral expression, with larger fish being more active and aggressive. Swimming activity and active aggression were positively correlated, forming a behavioral syndrome in the studied population. Based on these behavioral traits, we could also distinguish two behavioral clusters: one consisting of more active and aggressive individuals and the other consisting of less active and aggressive individuals. This indicates that brown trout fry adopt distinct behavioral strategies early in life.Significance statementThis paper provides information on the state-dependence of behavior in animals, in particular young brown trout. On the one hand, our data suggest a weak energetic state feedback where activity and aggression is increased as a response to short term food restriction. This suggests a limited scope for behavioral alterations in the face of starvation. On the other hand, body size is linked to higher activity and aggression, likely as a positive feedback between size and dominance. The experiment was carried out during the main population survival bottleneck, and the results indicate that growth is important during this stage, as 1) behavioral compensation to increase growth is limited, and 2) growth likely increases the competitive ability. However, our data also suggests that the population separates into two clusters, based on combined scores of activity and aggression (which are positively linked within individuals). Thus, apart from an active and aggressive strategy, there seems to be another more passive behavioral strategy.

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.

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Alternative migratory tactics in brown trout (Salmo trutta) are underpinned by divergent regulation of metabolic but not neurological genes.

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