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The circadian clock controls behavior and metabolism in various organisms. However, the exact timing and strength of rhythmic phenotypes can vary significantly between individuals of the same species. This is highly relevant for rhythmically complex marine environments where organismal rhythmic diversity likely permits the occupation of different microenvironments. When investigating circadian locomotor behavior of Platynereis dumerilii, a model system for marine molecular chronobiology, we found strain-specific, high variability between individual worms. The individual patterns were maintained for several weeks. A diel head transcriptome comparison of behaviorally rhythmic versus arrhythmic wild-type worms showed that 24-h cycling of core circadian clock transcripts is identical between both behavioral phenotypes. While behaviorally arrhythmic worms showed a similar total number of cycling transcripts compared to their behaviorally rhythmic counterparts, the annotation categories of their transcripts, however, differed substantially. Consistent with their locomotor phenotype, behaviorally rhythmic worms exhibit an enrichment of cycling transcripts related to neuronal/behavioral processes. In contrast, behaviorally arrhythmic worms showed significantly increased diel cycling for metabolism- and physiology-related transcripts. The prominent role of the neuropeptide pigment-dispersing factor (PDF) in Drosophila circadian behavior prompted us to test for a possible functional involvement of Platynereis pdf. Differing from its role in Drosophila, loss of pdf impacts overall activity levels but shows only indirect effects on rhythmicity. Our results show that individuals arrhythmic in a given process can show increased rhythmicity in others. Across the Platynereis population, rhythmic phenotypes exist as a continuum, with no distinct "boundaries" between rhythmicity and arrhythmicity. We suggest that such diel rhythm breadth is an important biodiversity resource enabling the species to quickly adapt to heterogeneous or changing marine environments. In times of massive sequencing, our work also emphasizes the importance of time series and functional tests., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Häfker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Many species synchronize their physiology and behavior to specific hours. It is commonly assumed that sunlight acts as the main entrainment signal for ∼24-h clocks. However, the moon provides similarly regular time information. Consistently, a growing number of studies have reported correlations between diel behavior and lunidian cycles. Yet, mechanistic insight into the possible influences of the moon on ∼24-h timers remains scarce. We have explored the marine bristleworm Platynereis dumerilii to investigate the role of moonlight in the timing of daily behavior. We uncover that moonlight, besides its role in monthly timing, also schedules the exact hour of nocturnal swarming onset to the nights’ darkest times. Our work reveals that extended moonlight impacts on a plastic clock that exhibits <24 h (moonlit) or >24 h (no moon) periodicity. Abundance, light sensitivity, and genetic requirement indicate that the Platynereis light receptor molecule r-Opsin1 serves as a receptor that senses moonrise, whereas the cryptochrome protein L-Cry is required to discriminate the proper valence of nocturnal light as either moonlight or sunlight. Comparative experiments in Drosophila suggest that cryptochrome’s principle requirement for light valence interpretation is conserved. Its exact biochemical properties differ, however, between species with dissimilar timing ecology. Our work advances the molecular understanding of lunar impact on fundamental rhythmic processes, including those of marine mass spawners endangered by anthropogenic change.

Genetic divergence of populations in the presence of gene flow is a central theme in speciation research. Theory predicts that divergence can happen with full range overlap - in sympatry - driven by ecological factors, but there are few empirical examples of how ecologically divergent selection can overcome gene flow and lead to reproductive isolation. In the marine midge Clunio marinus (Diptera: Chironomidae) reproduction is ecologically restricted to the time of the lowest tides, which is ensured through accurate control of development and adult emergence by circalunar and circadian clocks. As tidal regimes differ along the coastline, locally adapted timing strains of C. marinus are found in different sites across Europe. At the same time, ecologically suitable low tides occur at both full and new moon and twice a day, providing C. marinus with four nonoverlapping temporal niches at every geographic location. Along the coast of Brittany, which is characterized by a steep gradient in timing of the tides, we found an unusually large number of differentially adapted timing strains, and the first known instances of sympatric C. marinus strains occupying divergent temporal niches. Analysis of mitochondrial genotypes suggests that these timing strains originated from a single recent colonization event. Nuclear genotypes show strong gene flow, sympatric timing strains being the least differentiated. Even when sympatric strains exist in nonoverlapping temporal niches, timing adaptations do not result in genome-wide genetic divergence, suggesting timing adaptations are maintained by permanent ecological selection. This constitutes a model case for incipient ecological divergence with gene flow., (© 2021 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Starting with the beginning of the last century, a multitude of scientific studies has documented that the lunar cycle times behaviors and physiology in many organisms. It is plausible that even the first life forms adapted to the different rhythms controlled by the moon. Consistently, many marine species exhibit lunar rhythms, and also the number of documented "lunar-rhythmic" terrestrial species is increasing. Organisms follow diverse lunar geophysical/astronomical rhythms, which differ significantly in terms of period length: from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles). Evidence for internal circatital and circalunar oscillators exists for a range of species based on past behavioral studies, but those species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies. Thus, the underlying molecular mechanisms are largely obscure: the dark side of the moon. Here we review findings that start to connect molecular pathways with moon-controlled physiology and behaviors. The present data indicate connections between metabolic/endocrine pathways and moon-controlled rhythms, as well as interactions between circadian and circatidal/circalunar rhythms. Moreover, recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers. However, for each interpretation, it is important to carefully consider the, partly substantially differing, conditions used in each experimental paradigm. In the future, it will be important to use lab experiments to delineate the specific mechanisms of the different solar- and lunar-controlled rhythms, but to also start integrating them together, as life has evolved equally long under rhythms of both sun and moon., (Copyright © 2020 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

Many marine animals, ranging from corals to fishes, synchronise reproduction to lunar cycles. In the annelid Platynereis dumerilii, this timing is orchestrated by an endogenous monthly (circalunar) clock entrained by moonlight. Whereas daily (circadian) clocks cause extensive transcriptomic and proteomic changes, the quality and quantity of regulations by circalunar clocks have remained largely elusive. By establishing a combined transcriptomic and proteomic profiling approach, we provide first systematic insight into the molecular changes in Platynereis heads between circalunar phases, and across sexual differentiation and maturation. Whereas maturation elicits large transcriptomic and proteomic changes, the circalunar clock exhibits only minor transcriptomic, but strong proteomic regulation. Our study provides a versatile extraction technique and comprehensive resources. It corroborates that circadian and circalunar clock effects are likely distinct and identifies key molecular brain signatures for reproduction, sex and circalunar clock phase. Examples include prepro-whitnin/proctolin and ependymin-related proteins as circalunar clock targets., Competing Interests: SS, FS, DA, BM, AB, HM, Av, CG, FR, KT No competing interests declared, SB is affiliated with Lexogen GmbH. The author has no other competing interests to declare., (© 2019, Schenk et al.)

Organisms use endogenous clocks to anticipate regular environmental cycles, such as days and tides. Natural variants resulting in differently timed behaviour or physiology, known as chronotypes in humans, have not been well characterized at the molecular level. We sequenced the genome of Clunio marinus, a marine midge whose reproduction is timed by circadian and circalunar clocks. Midges from different locations show strain-specific genetic timing adaptations. We examined genetic variation in five C. marinus strains from different locations and mapped quantitative trait loci for circalunar and circadian chronotypes. The region most strongly associated with circadian chronotypes generates strain-specific differences in the abundance of calcium/calmodulin-dependent kinase II.1 (CaMKII.1) splice variants. As equivalent variants were shown to alter CaMKII activity in Drosophila melanogaster, and C. marinus (Cma)-CaMKII.1 increases the transcriptional activity of the dimer of the circadian proteins Cma-CLOCK and Cma-CYCLE, we suggest that modulation of alternative splicing is a mechanism for natural adaptation in circadian timing., Competing Interests: The authors declare no competing financial interests.

A quick guide into the new model annelid Platynereis., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Life is controlled by multiple rhythms. Although the interaction of the daily (circadian) clock with environmental stimuli, such as light, is well documented, its relationship to endogenous clocks with other periods is little understood. We establish that the marine worm Platynereis dumerilii possesses endogenous circadian and circalunar (monthly) clocks and characterize their interactions. The RNAs of likely core circadian oscillator genes localize to a distinct nucleus of the worm's forebrain. The worm's forebrain also harbors a circalunar clock entrained by nocturnal light. This monthly clock regulates maturation and persists even when circadian clock oscillations are disrupted by the inhibition of casein kinase 1δ/ε. Both circadian and circalunar clocks converge on the regulation of transcript levels. Furthermore, the circalunar clock changes the period and power of circadian behavior, although the period length of the daily transcriptional oscillations remains unaltered. We conclude that a second endogenous noncircadian clock can influence circadian clock function., (Copyright © 2013 The Authors. Published by Elsevier Inc. All rights reserved.)