Circadian Clocks in Fish—What Have We Learned so far?

Abstract

Zebrafish represent the one alternative vertebrate, genetic model system to mice that can be easily manipulated in a laboratory setting. With the teleost Medaka (Oryzias latipes), which now has a significant following, and over 30,000 other fish species worldwide, there is great potential to study the biology of environmental adaptation using teleosts. Zebrafish are primarily used for research on developmental biology, for obvious reasons. However, fish in general have also contributed to our understanding of circadian clock biology in the broadest sense. In this review, we will discuss selected areas where this contribution seems most unique. This will include a discussion of the issue of central versus peripheral clocks, in which zebrafish played an early role; the global nature of light sensitivity; and the critical role played by light in regulating cell biology. In addition, we also discuss the importance of the clock in controlling the timing of fundamental aspects of cell biology, such as the temporal control of the cell cycle. Many of these findings are applicable to the majority of vertebrate species. However, some reflect the unique manner in which “fish” can solve biological problems, in an evolutionary context. Genome duplication events simply mean that many fish species have more gene copies to “throw at a problem”, and evolution seems to have taken advantage of this “gene abundance”. How this relates to their poor cousins, the mammals, remains to be seen.

Comparative transcriptome analysis of wild and lab populations of Astyanax mexicanus uncovers differential effects of environment and morphotype on gene expression

“…As such it has been shown that 24‐hr rhythms in clock gene transcription are repressed in wild cave‐dwelling populations, however, in lab‐reared cavefish populations, transcriptional rhythms in core clock genes are present (Beale et al, 2013). Previous studies used fin tissue; leveraging the existence of autonomous cellular clocks spread throughout the body in teleosts (Froland Steindal & Whitmore, 2019; Whitmore, Foulkes, Strahle, & Sassone‐Corsi, 1998). However, clock gene expression can differ in the liver where the rhythmic expression of genes is central to energy homeostasis (Vollmers et al, 2009; Zwighaft, Reinke, & Asher, 2016).…”

Exposure to Artificial Light at Night and the Consequences for Flora, Fauna, and Ecosystems

“…In fish and lizards, the circadian system is made of a network of independent and interconnected light-sensitive oscillatory units located in the retina, the pineal gland and probably also in the brain ( Tosini et al, 2001 ; Falcón et al, 2007b ). Studies in the zebrafish indicated that virtually all cells from any tissue are light sensitive circadian oscillators ( Steindal and Whitmore, 2019 ), but the great variety of fish species precludes making any generalization. In any case, the pineal gland appears to act as a potent master oscillator, depending on the species ( Underwood, 1989 ; Whitmore et al, 1998 ; Figure 11 ).…”

“…The cardiovascular system (blood pressure and heart rate) and neuronal electrical activity (electroretinogram and electroencephalogram) do not escape the rule as they also fluctuate rhythmically ( Boissin and Canguilhem, 1998 ; Peters and Cassone, 2005 ; Cameron and Lucas, 2009 ; Talathi et al, 2009 ; Wood and Loudon, 2014 ; Petsakou et al, 2015 ; Cavey et al, 2016 ; Paul et al, 2016 ; Figure 11 and Table 1 ). Finally, in many tissues, clocks also control the cell division cycle ( Boissin and Canguilhem, 1998 ; Steindal and Whitmore, 2019 ), as well as some adaptive cellular movements including retino-motor movements (the respective elongation and retraction of cones and rods observed in fish and amphibians retinas at the L-to-D and D-to-L transitions) ( Kwan et al, 1996 ; Song et al, 2017 ). Accordingly, dozens of behavioural activities display daily and annual rhythms, including locomotor activity and sleep, schooling behaviour (fish), pigmentation or fur renewal, vertical (fish) and horizontal (all vertebrates) migration, behavioural thermoregulation (fish), vocalization (fish, birds), food intake, mating and reproduction, etc…( Zachmann et al, 1992 ; Lincoln et al, 2006 ; Cancho-Candela et al, 2007 ; Kantermann et al, 2007 ; Foster and Roenneberg, 2008 ; Kulczykowska et al, 2010 ; Cassone, 2014 ; Ruf and Geiser, 2015 ; Table 1 ).…”

Zebrafish Circadian Clock Entrainment and the Importance of Broad Spectral Light Sensitivity

“…It therefore came as a surprise, some 20 years ago, that the process of non-visual photoreception is something that all tissues in the zebrafish are capable of Whitmore et al (1998). Although the zebrafish pineal has key functions (Ben-Moshe et al, 2014;Livne et al, 2016), teleost clock systems appear to be highly decentralised, with all tissues and the majority of cells possessing a directly light entrainable circadian pacemaker (Whitmore et al, 1998(Whitmore et al, , 2000Carr and Whitmore, 2005;Tamai et al, 2005;Steindal and Whitmore, 2019).…”

“…Absorption spectra has been performed on many of these zebrafish opsins. Most are monophasic, but seemingly with somewhat broad absorption peaks, with most opsins absorbing in the blue-green, while some absorb up in the red end of the spectrum (Su et al, 2006;Davies et al, 2011Davies et al, , 2015Koyanagi et al, 2015;Morrow et al, 2016;Sato et al, 2016Sato et al, , 2018Sugihara et al, 2016;Steindal and Whitmore, 2019). Thus, the zebrafish has the theoretical capacity to detect light ranging from UV to IR and across the visual spectrum.…”