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

Abstract

Circadian rhythms and energy metabolism are critical and interconnected components of animal physiology. Metabolic inputs like time of feeding modulate circadian clocks and behavioral and molecular rhythms. In turn, circadian clocks regulate metabolic processes, allowing animals to optimize energy usage on daily timescales. On longer timescales, animals require physiological responses to tolerate variation in food availability. Most of our mechanistic knowledge of these processes comes from terrestrial mammals and insects, while there are major knowledge gaps for marine invertebrates. My dissertation focuses on the interactions of circadian rhythms and metabolism in three marine invertebrate systems using a combination of behavioral, molecular, and bioinformatic approaches. In Chapter 2, to understand how sensory signals are integrated into circadian clocks, I test the effects of various light and temperature regimes on circadian rhythms in the sea anemone Nematostella vectensis. Misaligned light and temperature cycles severely disrupt behavioral rhythms and substantially alter the rhythmic transcriptome, particularly the expression of genes mediating metabolic processes. This illustrates how interactions between environmental cues shape circadian behavior and physiology. In Chapter 3, I develop a high-throughput behavioral system to study diel vertical migration (DVM) in the copepod Acartia tonsa. DVM is driven by tradeoffs related to food availability, but we do not fully understand how food availability affects this circadian process. Using high-resolution tracking software, I find that Acartia possesses group-level DVM-like circadian rhythms in the lab, and that these swimming rhythms are altered by time-restricted feeding. This illustrates that food availability can impact DVM via effects on circadian clocks. In Chapter 4, I analyze how polar copepods respond to starvation at the molecular level. I find that two species with distinct dietary strategies partially share a genetic toolkit to respond to starvation, whereas differences in their starvation responses may reflect different modes of lipid storage. I also use evolutionary analyses to show that starvation response genes are under selective constraint, underlining their importance to organismal fitness. In aggregate, this thesis provides insights into the circadian rhythms of marine organisms, explores how metabolism modulates circadian rhythms, and sheds lights on the physiological consequences of food availability in zooplankton.