Biological clock function is linked to proactive and reactive personality types

Abstract

BackgroundMany physiological processes in our body are controlled by the biological clock and show circadian rhythmicity. It is generally accepted that a robust rhythm is a prerequisite for optimal functioning and that a lack of rhythmicity can contribute to the pathogenesis of various diseases. Here, we tested in a heterogeneous laboratory zebrafish population whether and how variation in the rhythmicity of the biological clock is associated with the coping styles of individual animals, as assessed in a behavioural assay to reliably measure this along a continuum between proactive and reactive extremes.ResultsUsing RNA sequencing on brain samples, we demonstrated a prominent difference in the expression level of genes involved in the biological clock between proactive and reactive individuals. Subsequently, we tested whether this correlation between gene expression and coping style was due to a consistent change in the level of clock gene expression or to a phase shift or to altered amplitude of the circadian rhythm of gene expression. Our data show a remarkable individual variation in amplitude of the clock gene expression rhythms, which was also reflected in the fluctuating concentrations of melatonin and cortisol, and locomotor activity. This variation in rhythmicity showed a strong correlation with the coping style of the individual, ranging from robust rhythms with large amplitudes in proactive fish to a complete absence of rhythmicity in reactive fish. The rhythmicity of the proactive fish decreased when challenged with constant light conditions whereas the rhythmicity of reactive individuals was not altered.ConclusionThese results shed new light on the role of the biological clock by demonstrating that large variation in circadian rhythmicity of individuals may occur within populations. The observed correlation between coping style and circadian rhythmicity suggests that the level of rhythmicity forms an integral part of proactive or reactive coping styles.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0618-0) contains supplementary material, which is available to authorized users.

Harvesting-induced evolution of collective risk-taking behavior and changes to the circadian system in a fish

“…These findings again suggested the evolution of a foraging-optimizing timing of activity, likely linked to boldness. Our finding are supported by a recent study demonstrating that proactive zebrafish (i.e., risk-taking individuals) are more active in the first hours of photophase compared to reactive ones (29). Relatedly, the self-feeding activity events of the small-harvested line extended to the hours before and after light-on.…”

“…Recent studies on zebrafish demonstrated that proactive and reactive phenotypes in zebrafish explain a large fraction of the variation of the brain transcriptome including expression of genes related to the circadian system (28). Moreover, proactive phenotypes were found to have more robust molecular (i.e., clock genes daily expression), humoral (i.e., daily secretion of melatonin) and behavioral (i.e., locomotor activity) oscillations of the circadian system (29). However, both of the cited studies measured transcripts abundance under LD conditions; therefore the truly endogenous nature of the circadian molecular clockwork could have been masked by the LD cycle.…”

“…These data collectively provided strong evidence that size-selection over just five generations affected both genes and phenotypes, suggesting that size-selection could also have left a molecular legacy in the circadian system. In the present work, we test the hypothesis that risk taking behavior and the circadian system share common pathways (29) and we predicted that harvesting-induced evolution of risk-taking behavior has altered the circadian system in the zebrafish selection lines. We also expected that possible changes in shoaling behavior (i.e., sociability; 19) would affect the social synchronization of individual circadian clocks (Bloch et al, 2013), with consequent changes in the collective circadian output at the group level.…”

“…Functional circadian clocks are essential for precise timing of activity, thereby helping the organism to avoid or minimize risk of predation while maximizing foraging (27). Recent studies reported an insofar unknown relationship of animal personality, particularly an animal’s tendency to take risks, and the circadian system (28, 29) suggesting genetic correlations among traits. Zebrafish ( Danio rerio ) of different coping styles, commonly referred to as proactive/reactive behavioural phenotypes (30), were found to be systematically linked to different properties of circadian rhythms (29).…”

“…Recent studies reported an insofar unknown relationship of animal personality, particularly an animal’s tendency to take risks, and the circadian system (28, 29) suggesting genetic correlations among traits. Zebrafish ( Danio rerio ) of different coping styles, commonly referred to as proactive/reactive behavioural phenotypes (30), were found to be systematically linked to different properties of circadian rhythms (29). Moreover, life history changes correlate with the circadian clock (e.g., 31, 32).…”