Differential responses to environmental challenge by common carp Cyprinus carpio highlight the importance of coping style in integrative physiology

Abstract

Common carp Cyprinus carpio displaying proactive or reactive stress coping styles were acclimated to two environmental regimes (low oxygen and low temperature), and selected groups were tested for response to an inflammatory challenge (Escherichia coli lipopolysaccharide, LPS). Plasma glucose and lactate levels were measured, as were selected C. carpio-specific messenger (m)RNA transcript abundance, including cortisol receptor (CR), enolase (ENO), glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and interleukin-1-beta (IL1β) was measured in individual whole brain samples. Basal levels (in sham injected fish held in normoxic conditions at 25° C) of plasma lactate and glucose differed between coping styles, being significantly lower in proactive individuals. Both variables increased in response to LPS challenge, with the exception of plasma glucose in reactive fish held in hypoxia. Baseline levels of gene expression under control conditions were significantly different for GAPDH between behavioural phenotypes. The responses to experimental challenge were sometimes diametrically opposed between stress-coping styles in a transcript-specific manner. For CR and GAPDH, for example, the response to LPS injection in hypoxia were opposite between proactive and reactive animals. Proactive fish showed decreased CR and increased GAPDH, whereas reactive showed the opposite response. These results further highlight that screening for stress-coping styles prior to experiments in adaptive physiology can significantly affect the interpretation of data obtained. Further, this leads to a more finely tuned analytical output providing an improved understanding of variation in individual responses to both environmental and inflammatory challenge.

Temperature Preference and Sex Differentiation in African Catfish, Clarias gariepinus

“…Rey et al. (, ) also showed that proactive fish generally have an explorative behavior and a preference for higher temperature environments, when reactive animals are shyer and spent more time in lower water temperatures. Our study showed a high variability in temperature preference according to the period (before, during, and after high thermosensitive period) and the progenies.…”

On the Role of Neurogenesis and Neural Plasticity in the Evolution of Animal Personalities and Stress Coping Styles

“…Among the questions raised are: via what mechanisms are trait correlations inherited, which circumstances benefit different complex phenotypes, and what are the costs and benefits of the limited plasticity imposed by fixed trait associations? In the bioinformatics era, it should also be noted that understanding individual variation may be of vital importance for the interpretation of transcriptomic data [see for example Crawford and Oleksiak, 2008;MacKenzie et al, 2009;Wong et al, 2015;Rey et al, 2016].…”

Reproduction, olfaction and dominance behaviour in Senegalese sole (Solea senegalensis)

“…Differences in metabolism have been linked with changes in coping styles in some species (Biro and Stamps, 2008;. In relation to the stress coping style biomarkers, the literature is scarce, however some studies have been performed in fish, such as, zebrafish ), common carp (MacKenzie et al, 2009Rey et al, 2016), Nile tilapia (Oreochromis niloticus) (Vera Cruz and Brown, 2007), rainbow trout (Thomson et al, 2011) associating physiological and brain gene expression characteristics with behavioural phenotype.…”

“…The information of these mRNAs differentially expressed between diverse SCS groups could be used for the interpretation of biological responses to resolve variation, knowing that those variations might be adaptive or genetically fixed within the population (MacKenzie et al, 2009). As commented before, the behavioural features are connected to physiological characteristics and related to this physiological association, recent molecular measurements have been associated with behavioural coping styles in response to fluctuating environmental conditions and after an inflammatory challenge in several fish species MacKenzie et al, 2009;Huntingford et al, 2010;Rey et al, 2013;Rey et al, 2016).…”

“…The knowledge of coping styles in fish has high importance, not only from an evolutionary perspective but also for aquaculture, in order to increase productivity and to aid genetic breeding programs achieve improved survival, growth and enhanced immune responses . For example, some researchers demonstrated that proactive fish tended to possess a higher immune reaction (MacKenzie et al, 2009;Rey et al, 2016), higher growth rates (Millot et al, 2009), and higher reproductive success (Godin and Dugatkin, 1996), however, showed lower anti-predatory responses than reactive fish (Huntingford et al, 2010). Physiologically, proactive fish have a lower activity at hypothalamus-pituitary-adrenal/interrenal (HPI) level, which affects the stress response to different stressors, presenting lower post-stress levels of glucocorticoids, which may be broadly classified to affect two major categories, immunological and metabolic response Braithwaite et al, 2011).…”