Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis

Abstract

Circadian clocks infer time of day by integrating information from cyclic environmental factors called zeitgebers, including light and temperature. Single zeitgebers entrain circadian rhythms, but few studies have addressed how multiple, simultaneous zeitgeber cycles interact to affect clock behavior. Misalignment between zeitgebers ('sensory conflict') can disrupt circadian rhythms, or alternatively clocks may privilege information from one zeitgeber over another. Here, we show that temperature cycles modulate circadian locomotor rhythms in Nematostella vectensis, a model system for cnidarian circadian biology. We conduct behavioral experiments across a comprehensive range of light and temperature cycles and find that Nematostella's circadian behavior is disrupted by chronic misalignment between light and temperature, which involves disruption of the endogenous clock itself rather than a simple masking effect. Sensory conflict also disrupts the rhythmic transcriptome, with numerous genes losing rhythmic expression. However, many metabolic genes remained rhythmic and in-phase with temperature, and other genes even gained rhythmicity, implying that some rhythmic metabolic processes persist even when behavior is disrupted. Our results show that a cnidarian clock relies on information from light and temperature, rather than prioritizing one signal over the other. Although we identify limits to the clock’s ability to integrate conflicting sensory information, there is also a surprising robustness of behavioral and transcriptional rhythmicity.

Feeding status modulates diel vertical migration of zooplankton via effects on circadian rhythms

“…We found that daytime feeding (DF) abolished DVM-like behavior. This is similar to other studies of "sensory conflict," whereby mismatches between two zeitgebers disrupt or weaken normal behavioral rhythms (Berger & Tarrant, 2023;Harper et al, 2016). DF copepods also displayed altered free-running rhythms, with notably longer periods than NF animals (28 h -30 h).…”

Exploring circadian rhythms, food intake, and their interactions in marine invertebrates

“…We found that daytime feeding (DF) resulted in a loss of DVM-like behavior. This is similar to other studies of "sensory conflict," whereby mismatches between two zeitgebers disrupt or weaken normal behavioral rhythms (Berger & Tarrant, 2023;Harper et al, 2016). DF copepods also displayed altered free-running rhythms, with notably longer periods than NF animals (28-30 h).…”

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

“…Investigating the factors that shape phenotypic and rhythmic diversity in an integrative way will help to understand how animals adapt to specific habitats and how these factors can contribute to overall population fitness. Differences between individuals and between levels of organization are common features of biological rhythm in various clades and habitats [59,[70][71][72], and individual differences in behavioral patterns directly feed back to the experienced ("realized") environmental cycles used for entrainment [73][74][75]. It is thus important to treat biological variation not as "background noise," but as an additional aspect of biodiversity that needs to be considered in both the mechanistic and the ecological context [28,76].…”

“…Of note, a study under sensory temporal conflict conditions in the sea anemone Nematostella vectensis showed that a misalignment of environmental light and temperature cycles resulted in disruption of the circadian behavior [ 59 ]. However, despite the arrhythmic behaviors under sensory conflict conditions, the number of 24-h cycling transcripts was similar to the control conditions, with less than half overlapping.…”