Circadian Clock Involvement in Zooplankton Diel Vertical Migration

Abstract

Biological clocks are a ubiquitous ancient and adaptive mechanism enabling organisms to anticipate environmental cycles and to regulate behavioral and physiological processes accordingly [1]. Although terrestrial circadian clocks are well understood, knowledge of clocks in marine organisms is still very limited [2-5]. This is particularly true for abundant species displaying large-scale rhythms like diel vertical migration (DVM) that contribute significantly to shaping their respective ecosystems [6]. Here we describe exogenous cycles and endogenous rhythms associated with DVM of the ecologically important and highly abundant planktic copepod Calanus finmarchicus. In the laboratory, C. finmarchicus shows circadian rhythms of DVM, metabolism, and most core circadian clock genes (clock, period1, period2, timeless, cryptochrome2, and clockwork orange). Most of these genes also cycle in animals assessed in the wild, though expression is less rhythmic at depth (50-140 m) relative to shallow-caught animals (0-50 m). Further, peak expressions of clock genes generally occurred at either sunset or sunrise, coinciding with peak migration times. Including one of the first field investigations of clock genes in a marine species [5, 7], this study couples clock gene measurements with laboratory and field data on DVM. While the mechanistic connection remains elusive, our results imply a high degree of causality between clock gene expression and one of the planet's largest daily migrations of biomass. We thus suggest that circadian clocks increase zooplankton fitness by optimizing the temporal trade-off between feeding and predator avoidance, especially when environmental drivers are weak or absent [8].

Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks

“…; Table ). This suggests that the diel rhythmic output of the clock was actively “switched off” during diapause and that arrhythmicity was not just a consequence of the lack of light at depth, as also supported by the observation that in C. finmarchicus clock genes continue diel cycling in constant darkness (Häfker et al ). As gene expression was determined from pooled individuals and because repeated measurements of the same individuals were not possible, the possibility that clocks remained rhythmic during diapause, but were desynchronized between individuals cannot be discounted.…”

“…However, the sampling interval (4 h) was too long to reliably test for this model. While 24‐h cycling was only found in clock genes but not in any other genes, it is probable that the clock also controls diel physiological rhythms such as respiration (Häfker et al ) or enzyme activity associated with nocturnal feeding (Båmstedt ) via downstream genes that then trigger cellular signal cascades regulating metabolic processes (Ceriani et al ; Panda et al ). These cascades may influence protein synthesis or enzyme activity (Panda et al ; Reddy and Rey ; Thurley et al ) explaining the lack of diel cycles in metabolic gene expression.…”

“…Maps were created with Ocean Data View v. 4.7.4 (Schlitzer 2015). Figure adopted and changed from Häfker et al ().…”

“…CTD hauls additionally provided high resolution profiles of ( B ) temperature, ( C ) salinity, ( D ) oxygen concentration, and ( E ) Chl a concentration for each seasonal time point. CTD data for May were previously shown in Häfker et al ().…”

Environmental Stress Responses and Experimental Handling Artifacts of a Model Organism, the Copepod Acartia tonsa (Dana)

“…The limited response at the transcriptional level 15 min following exposure to handling stress suggests that organisms collected in plankton tows of short duration and immediately used in incubation experiments or being preserved are likely to exhibit transcriptional profiles that represent their in situ physiological state (e.g., Häfker et al, 2017). It is, however, important to be aware of that handling has the potential to affect gene expression regardless of animal species.…”