Transcriptomics reveals that the caudal neurosecretory system in the olive flounder (Paralichthys olivaceus) is more responsive in bold individuals and to chronic temperature change

Abstract

In farmed animals, personalities have demonstrated links to performance traits, health and welfare, disease susceptibility, and to coping with environmental stress. The teleost caudal neurosecretory system (CNSS) of the posterior spinal cord is involved in the regulation of the osmoregulatory and stress responses and can directly sense a hypothermal challenge via a transient receptor potential ion channel. Here we investigated the global transcriptomic response of the CNSS of shy and bold individuals of the olive flounder (Paralichthys olivaceus) acclimated to 18 °C and transferred to 12 °C (low temperature treatment, LT) or 24 °C (high temperature treatment, HT) for 2 h (acute) or 8 days (chronic) in relation to fish maintained at 18 °C (control). Overall, differential transcriptomic responses were stronger in bold individuals and induced by acute HT and chronic LT treatments. Acute HT induced innate immunity, circadian rhythm, and cellular stress response pathways and, specifically in bold individuals, a heightened response of molecular chaperones of cellular response to heat which may be related to the mechanisms of rescue of downregulated RNA splicing processes. Chronic LT also caused downregulation of innate immunity pathways as well as pathways related to cell division. In addition, the CNSS of bold individuals was enriched in pathways related to regulation of cell cycle, adaptive immune response, and apoptosis, while cellular metabolism pathways were downregulated in shy individuals. The putative temperature sensor genes Trpv1 and Trpa1 were upregulated, respectively, after acute HT and chronic LT treatments, but there was no indication of a specific neurosecretory response of the CNSS. While several of the observed transcriptomic responses to temperature appear to be shared by other tissues and species, it is also clear that bold and shy behavioural personalities show marked different responses, with bold individuals the most responsive. These results add to the knowledge base available on olive flounder aquaculture, indicating a differential role of the CNSS in the response to temperature change according to behavioural personalities.