Analysis across diverse fish species highlights no conserved transcriptome signature for proactive behaviour

Background Consistent individual differences in behaviour, known as animal personalities, have been demonstrated within and across species. In fish, studies applying an animal personality approach have been used to resolve variation in physiological and molecular data suggesting a linkage, genotype-phenotype, between behaviour and transcriptome regulation. In this study, using three fish species (zebrafish; Danio rerio, Atlantic salmon; Salmo salar and European sea bass; Dicentrarchus labrax), we firstly address whether personality-specific mRNA transcript abundances are transferrable across distantly-related fish species and secondly whether a proactive transcriptome signature is conserved across all three species. Results Previous zebrafish transcriptome data was used as a foundation to produce a curated list of mRNA transcripts related to animal personality across all three species. mRNA transcript copy numbers for selected gene targets show that differential mRNA transcript abundance in the brain appears to be partially conserved across species relative to personality type. Secondly, we performed RNA-Seq using whole brains from S. salar and D. labrax scoring positively for both behavioural and molecular assays for proactive behaviour. We further enriched this dataset by incorporating a zebrafish brain transcriptome dataset specific to the proactive phenotype. Our results indicate that cross-species molecular signatures related to proactive behaviour are functionally conserved where shared functional pathways suggest that evolutionary convergence may be more important than individual mRNAs. Conclusions Our data supports the proposition that highly polygenic clusters of genes, with small additive effects, likely support the underpinning molecular variation related to the animal personalities in the fish used in this study. The polygenic nature of the proactive brain transcriptome across all three species questions the existence of specific molecular signatures for proactive behaviour, at least at the granularity of specific regulatory gene modules, level of genes, gene networks and molecular functions

Physiological responses during acute stress recovery depend on stress coping style in European sea bass, Dicentrarchus labrax

Individual stress coping style (reactive, intermediate and proactive) was determined in 3 groups of 120 pit tagged European seabass using the hypoxia avoidance test. The same three groups (no change in social composition) were then reared according to the standards recommended for this species. Then, 127 days later, individuals initially characterized as reactive, intermediate or proactive were submitted to an acute confinement stress for 30 min. Blood samples were taken to measure plasma cortisol levels 30 min (Stress30) or 150 min (Stress150) after the end of the confinement stress. Individuals were then sacrificed to sample the telencephalon in order to measure the main monoamines and their catabolites (at Stress30 only). Individuals from Stress150 were sampled for whole brain for a transcriptomic analysis. The main results showed that reactive individuals had a lower body mass than intermediate individuals which did not differ from proactive individuals. The physiological cortisol response did not differ between coping style at Stress30 but at Stress150 when intermediate and proactive individuals had recovered pre stress levels, reactive individuals showed a significant higher level illustrating a modulation of stress recovery by coping style. Serotonin turnover ratio was higher in proactive and reactive individuals compared to intermediate individuals and a significant positive correlation was observed with cortisol levels whatever the coping style. Further, the confinement stress led to a general increase in the serotonin turnover comparable between coping styles. Stress150 had a significant effect on target mRNA copy number (Gapdh mRNA copy number decreased while ifrd1 mRNA copy number increased) and such changes tended to depend upon coping style

Aerobic swimming in intensive finfish aquaculture: applications for production, mitigation and selection

We review knowledge on applications of sustained aerobic swimming as a tool to promote productivity and welfare of farmed fish species. There has been extensive interest in whether providing active species with a current to swim against can promote growth. The results are not conclusive but the studies have varied in species, life stage, swimming speed applied, feeding regime, stocking density and other factors. Therefore, much remains to be understood about mechanisms underlying findings of ‘swimming‐enhanced growth’, in particular to demonstrate that swimming can improve feed conversion ratio and dietary protein retention under true aquaculture conditions. There has also been research into whether swimming can alleviate chronic stress, once again on a range of species and life stages. The evidence is mixed but swimming does improve recovery from acute stresses such as handling or confinement. Research into issues such as whether swimming can improve immune function and promote cognitive function is still at an early stage and should be encouraged. There is promising evidence that swimming can inhibit precocious sexual maturation in some species, so studies should be broadened to other species where precocious maturation is a problem. Swimming performance is a heritable trait and may prove a useful selection tool, especially if it is related to overall robustness. More research is required to better understand the advantages that swimming may provide to the fish farmer, in terms of production, mitigation and selection

Individual fish rhythm directs group feeding: a case study with sea bass juveniles (

The long term influence of individual biological rhythms on group feed demand behaviour was investigated in European sea bass (Dicentrarchus labrax) held under controlled environmental conditions with an on-demand feeding system. The experiment was realized over 219 days with 190 fish distributed on 4 tanks. Sea bass had a mean body mass comprised between 139 g to 183 g. The number of feed demand acts by each individual was calculated daily, and the population could thus be partitioned into three categories (high-, low- and zero-triggering fish). The duration of the period that an individual held high-triggering status could vary, but was 63 ± 16 days on average. The transition period between two highest-triggering fish in one tank was on average 4 ± 4 days. The group feeding rhythm followed the same pattern of feed demand rhythm as the highest-triggering individual fish. When the highest-triggering fish was nocturnal, the totality of feed demand in the group was realized during the night with one peak at 22:00, corresponding to dusk under experimental conditions. When the highest-triggering fish was diurnal, the majority of feed demand in the group was realized during the light period with one peak at 06:00, corresponding to dawn, and/or another at 12:00. This study therefore highlights that sea bass group feeding behaviour is not the sum of individual feed demand behaviours, but is directed by the rhythm and behaviour of a few high-triggering fish. The regular changes of high-triggering fish in the group proved that it was not the identity of these particular fish that was most important for the group, but their role as a feed demand leader

Response to visual and mechano-acoustic predator cues is robust to ocean warming and acidification and is highly variable in European sea bass

Predator-prey interactions and, especially, the success of anti-predator responses are modulated by the sensory channels of vision, olfaction, audition and mechanosensation. If climate change alters fish sensory ability to avoid predation, community dynamics can be affected. We investigated whether mid-duration exposure to warming and/or acidification alters behavioural response to visual or mechano-acoustic predator cues in juvenile Dicentrarchus labrax. We measured kinematic variables before and after a visual or a mechano-acoustic challenge which mimicked an overflying bird shadow or a bird swoop attack, respectively. Due to large interindividual variability in responses before cue presentation, fish were categorized as slow and fast to account for baseline individual variability. Treatment did not impact kinematic variables as both slow and fast fish of every treatment elicited precautionary and escape responses. Interestingly, even slow fish swam as fast as fast fish after the cue, suggesting that regardless of initial category, fish managed to escape facing a danger. Anti-predator response varied according to the level of threat to survival with greater responses elicited after the swoop attack. Although wild juvenile sea bass aggregate in schools, school dynamics rely on single leaders which highlights the importance of the variability in individual behaviours. We demonstrated that anti-predator response in juvenile D. labrax is robust to mid-duration exposure to independent and combined effects of warming and acidification. If robustness is confirmed over long-duration, it could provide D. labrax with an evolutionary advantage in the future ocean, where cue transmission through changing environments can further modulate cue perception and predator-prey interactions

Spatial distribution and activity patterns as welfare indicators in response to water quality changes in European sea bass, Dicentrarchus labrax

International audienceIn aquaculture,fish are exposed to unavoidable stressors that can be detrimental for their health and welfare.However, welfare in farmedfish can be difficult to assess, and, so far, no standardized test has been universallyaccepted as a welfare indicator. This work contributes to the establishment of behavioural welfare indicators in amarine teleost in response to different water quality acute stressors. Groups of tenfish were exposed to highTotal Ammonia Nitrogen concentration (High TAN, 18 mg.L-1), Hyperoxia (200 % O2saturation), Hypoxia (20 %O2saturation), or control water quality (100% O2saturation and TAN < 2.5 mg.L-1) over 1 hour. Fish were thentransferred in a novel environment for a group behaviour test under the same water quality conditions over 2hours. Videos were recorded to assess thigmotaxis, activity and group cohesion. After this challenge, plasmacortisol concentration was measured in a subsample, while individual behavioural response was measured in theotherfish using novel tank diving test. Prior to this study, the novel tank diving test was validated as a beha-vioural challenge indicative of anxiety state, by using nicotine as anxiolytic drug. Overall, all stress conditionsinduced a decrease in activity and thigmotaxis and changes in group cohesion while onlyfish exposed toHypoxia and High TAN conditions displayed elevated plasma cortisol concentrations. Inpost-stress condition,activity was still affected but normal behaviour was recovered within the 25 minutes of the test duration. Ourwork suggests that the activity, thigmotaxis and group cohesion are good behavioural indicators of exposure todegraded water quality, and could be used as standardized measures to assessfish welfare

Self-feeding behavior changes induced by a first and a second generation of domestication or selection for growth in the European sea bass,

Among the strategies that can be used to improve fish welfare in a rearing environment, domestication and/or selective breeding was proposed to minimize fish responsiveness to husbandry practices. To verify this hypothesis on a recently domesticated species, the sea bass Dicentrarchus labrax, two experiments were realized, each using two populations differing according to their level of domestication or selection. For the first experiment, we used one population produced from wild parents (Wild; initial body mass: 106  ±  3 g), and one population from parents selected for growth for one generation (Selected 1; initial body mass: 129  ±  4 g). For the second experiment, we used one population produced from parents domesticated for two generations (Domesticated; initial body mass: 72  ±  3 g), and one produced from parents selected for growth for two generations (Selected 2; initial body mass: 89  ±  4 g). The first experiment was carried out over 112 days with 240 fish (60 fish per tank, 120 fish per population), and the second one over 84 days with 200 fish (50 fish per tank, 100 fish per population). Two variables, self-feeding behavior and growth performance, were measured over the time of the experiments. After a control period, the fish were submitted twice, at three-week intervals, to an acute stress treatment consisting of draining the tank and leaving the fish out of water for one minute. Both self-feeding behavior and growth performance were altered by the acute stress treatment. During the first post-stress period, the Domesticated and Selected (1 and 2) groups showed more pronounced post-stress exposure responses than the Wild fish: they modified their feeding rhythm, their feed intake, and their growth rate. During the second post-stress period, feeding rhythm was still affected (being more diurnal with a well defined peak), but the feed intake and growth rate results showed that the Domesticated and Wild groups seemed less affected than the Selected (1 and 2) populations, which continued to express a high post-stress response. According to these results, it can be concluded that: (1) an application of two acute stress treatments, at three-week intervals, modified fish feeding behavior and growth performance; (2) the domestication process seemed to improve fish adaptation abilities to this kind of stress; and (3) the process of selection for growth led to a final, better growth, but did not seem to improve fish acute stress tolerance