BSci 3230 Tidal & Lunar Rhythms PDF

NOTE ! These files are provided for the sole purpose of assisting BSci 3230 students to study for exams in the class. Some of the material in these files may be copyrighted, and it is not OK for you to share these files with anyone who is not a student in this class or to use them for any purpose ot...

NOTE ! These files are provided for the sole purpose of assisting BSci 3230 students to study for exams in the class. Some of the material in these files may be copyrighted, and it is not OK for you to share these files with anyone who is not a student in this class or to use them for any purpose other than to study for BSci 3230. Thanks, Carl Johnson  BSci 3230 Tidal and Lunar Rhythms What is the relationship between the circadian clockwork and the mechanism(s) underlying circa-tidal and circa-lunar rhythms? Circatidal/circadian comparison, example: the crustacean Eurydice. Circalunar examples: lunar spawning (corals) the midge (fly) Clunio marinus the marine annelid worm Platynereis Humans ? (!) Note: many of the slides included in this lecture are courtesy of Dr. Bambos Kyriacou, University of Leicester, U.K. Tidal environments  Tidal environments Bay of Fundy, Canada High Tide Low Tide Tidal environments Earth, moon, and sun lead to lunar and tidal rhythms Tidal rhythms Tidal period is 12.4 h, but consecutive cycles may have different height/trough values Tidal rhythms NT ST ST NT ST = Spring Tide NT = Neap Tide  Models of the clockwork driving “tidal” rhythms In the intertidal zone, both the phase of the tide and the phase of the light/dark cycle are important in predator/prey & foraging relationships, so a clock to anticipate high & low tides could be valuable. Is the mechanism of the tidal clock fundamentally a slightly lengthened circadian oscillator with two peaks ? Or does the tidal clock have an independent biochemical mechanism with a 12.4 h period ? Quote from Dr. Kyriacou: “60 years of research and still no idea... we need a model organism(s) to study”  Eurydice pulchra* In Greek mythology, Eurydice was one of the daughters of Apollo. She was the wife of Orpheus, who tried to bring her back from the dead with his enchanting music. 1mm *Eurydice is an isopod crustacean related to shrimps, crayfish, crabs, lobsters, etc.  Eurydice pulchra* Eurydice pulchra as a “model” tidal organism Bangor 1mm U.K. *Eurydice is an isopod crustacean related to shrimps, crayfish, crabs, lobsters, etc.  Tidal Swimming Cycles 24.8 Double-plotted Double-plotted Periodogram on 12.4 h scale on 24 h scale analysis Period (Tau, t) of swimming rhythm is temperature compensated Zhang et al 2013 Curr Biol Tidal Swimming Cycles Swimming rhythm can be entrained by a cycle of vibration (red arrows) Zhang et al 2013 Curr Biol  Eurydice ALSO have circadian cycles in chromatophore dispersion Anticipated light schedule on beach 5 ~ 24 hours Chromatophore index 4 3 2 1 13 16 19 22 01 04 07 10 13 16 19 22 01 I II III IV V Solar time This rhythm can be entrained by L/D cycles, but not by vibration cycles Zhang et al 2013 Curr Biol  Rationale Eurydice show tidal and circadian phenotypes If the underlying molecular basis of circatidal rhythms depends on circadian clock proteins then...... disrupting clock proteins genetically or environmentally should affect both phenotypes.  Clock gene expression (mRNA abundance) only Eptim mRNA cycles in head...this might be a molecular circadian phenotype? Circadian chromatophore and Eptim mRNA cycles are disrupted in LL... LL DD... but tidal swimming t is only slightly FRP of swimming rhythm shortened Zhang et al 2013 Curr Biol  ”Knock down” Epper mRNA expression with ds RNAi control dsRNAi to Epper t of swimming rhythm (h) t of circatidal swimming rhythm is unaffected by Epper RNAi, but circadian chromatophore and Eptim mRNA rhythms are blunted Eurydice circadian clock uses CRY2 as main negative regulator and BMAL1 as positive regulator TIM PER CRY2 CLK BMAL1 per/Cry (E-box) Zhang et al 2013 Curr Biol  Eurydice circadian clock uses CRY2 as main negative regulator and BMAL1 as positive regulator TIM PER CRY2 CLK BMAL1 per/Cry (E-box) PER CK1e CRY2 TIM Zhang et al 2013 Curr Biol  Therefore.... LL and knocking down Epper shortens/disrupts circadian rhythms in chromatophores and blunts the Eptim mRNA rhythm... BUT, tidal periodicity is maintained, suggesting INDEPENDENT MOLECULAR MECHANISMS However... Effects of Casein kinase 1 (CK1) inhibitors (PF480 & PF670) on circadian rhythms Reduction in amplitude and lengthening of period by the CK1 inhibitor PF670 Zhang et al 2013 Curr Biol CK1e/d inhibitors also affect tidal swimming period and circadian modulation Zhang et al 2013 Curr Biol  Therefore... Disrupting positive regulators with CK1ε/δ inhibitors affects BOTH TIDAL AND CIRCADIAN RHYTHMS, suggesting that the clocks underlying these two rhythms may share some molecular components. These and other data suggests a model for the tidal rhythm clock...  The putative tidal oscillator Hypothesis: the tidal clock of Eurydice uses VIB the same positive regulators as the ? CRY2? circadian clock but different negative regulators. One of the negative regulators + CLK BMAL1 (“blue ?” in the figure) may have a circatidal 12.4 or circalunidian 24.8 h (E-box) cycle of degradation rate and the overall tidal clock system might be reset by vibration via a vibration sensitive ? molecule, VIB CK1e ? VIB Zhang et al 2013 Curr Biol  induced ecological effects, such as species range expansion, decline in sea ice extent, and mass Lunar spawning rhythms bleaching of tropical coral reefs (6–8), are well studied and receive global attention, whereas phenological changes remain poorly understood. There are a number of spectacular Additionally, examples most of the studies of on phenological animals that spawn at ahave changes specific relatedphase temporal ofshifts the to mis- lunar cycle––formatched example, corals.orThis interactions mismatched synchrony phenomenon R ES E A RC H allowsbetween thespecies animals or trophic to spawnlevels (e.g., consumer- prey, hatchling–food source, plant-pollinator) synchronously, thereby enhancing the probability (1–4). ◥Here, we focus on mismatches of population- en ofR Efertilization and S E A R C H A R T Ilevel successful reproduction. C L E reproductive-phenology of reef-building (27 qu corals in the Gulf of Eilat (also referred to as the an CORAL REEFS on Gulf of Aqaba) in the Red Sea (fig. S1) and show Re that the once highly synchronized, iconic spawn- Breakdown in spawning synchrony: ing events of certain corals have lost synchrony, dif og A silent threat to coral persistence (21 and we examine the demographic consequences. syn Coral spawning is often presented as a prom- an co Tom Shlesinger* and Yossiinent Loya example of synchronized phenomena in an The impacts of human and nature. Coral colonies natural disturbances spanning on coral vast areas re- reefs are typically Co quantified through visiblelease damagetheir (e.g.,reproductive material reduced coral coverage as simultaneously a result of Th bleaching events), but changes in environmental conditions may also cause into damage in less visible ways. the water Despite column the current (fig. paradigm, S2 suggests which and movie S1), tan du consistent, highly synchronized spawning events, corals that reproduce by on broadcast spawning are particularly vulnerable because their reproductive sev phenology is governed by environmental cues. Here, we quantify coral spawning sp intensity during four annual reproductive seasons, alongside laboratory analyses oc at the polyp, colony, and School populationof Zoology, George levels, and S. Wise Faculty we demonstrate of compared that, Life Sciences, Su Tel-Aviv with historical data, several University, species from theTel-Aviv Red Sea69978, Israel have lost their reproductive bu synchrony. Ultimately, such a synchrony author. *Corresponding breakdown Email:reduces the probability [email protected] mo of successful fertilization, leading to a dearth of new recruits, which may drive Fo aging populations to extinction. ea of Shlesinger any of the coherent ecological et al., where impacts Sciencethe365, gametes1002–1007 (2019) remain viable for only6a Septe wi of climate change are reflected in shifts few hours (9, 10). Successful fertilization, which va in animal and plant phenology (i.e., the only takes place within this narrow time frame on  Lunar spawning rhythms Grunion are a hotdog-sized fish that spawn late at night on beaches in California and Baja California. The moon plays a very important role: grunions emerge out of the ocean and onto the beaches to spawn when the tides are at their highest––during the full moon and the new moon. At these times, grunions come up completely out of the water to lay and fertilize their eggs in the sand above the high tide line. This ensures that the eggs will only be submerged during high tides, which is important because it allows them to get enough oxygen. Being buried in sand also protects them from aquatic predators that would eat eggs floating in the water. Lunar spawning rhythms in the marine midge Clunio marinus In Clunio, larvae and pupae are submerged (for protection from predators?). During full and new moon, millions of male and female adults of the midge hatch from the pupal case to spawn as low tide exposes the habitats where they have developed from eggs to pupae. Why do you think this behavior follows the lunar cycle and entrains to the moon’s phase? NT = neap tide ST = spring tide ST ST tidal height NT NT adults mating hatching larvae hatching Lunar spawning rhythms in the marine midge Clunio marinus In Clunio, larvae and pupae are submerged (for protection from predators?). During full and new moon, millions of male and female adults of the midge hatch from the pupal case to spawn as low tide exposes the habitats where they have developed from eggs to pupae. These adults live for only a few hours after emergence, so it is critical that they hatch synchronously during those few hours of low tide to mate (and then die). NT = neap tide ST = spring tide ST ST tidal height NT NT adults mating hatching larvae hatching  Geographical variability in the timing of Clunio emergence “Por” “Jean” Circadian timing (phase) is critical and varies in different populations as does circalunar timing (1 vs. 2 peaks/month). Port-en-Bessin (Por) vs. St Jean (Jean) populations look very different in both time domains Kaiser et al. Nature 2016 Daily phase angle of circadian emergence time correlates (weakly?) with FRP Por Jean Port-en-Bessin (Por) populations emerge earlier in the day (phase) and have a shorter FRP, whereas St. Jean (Jean) populations emerge later in the day (phase) and have a longer FRP (FRP of adult emergence measured in dim LL) Kaiser et al. Nature 2016 Genetic mapping Port-en-Bessin vs. St Jean populations Quantitative Trait Locus (QTL) mapping gave one overlapping circadian phase/lunar pattern QTL (C1/L1) , a second circadian phase QTL (C2) and a third lunar pattern QTL (L2). None of the “canonical core” circadian clock genes were found to be located within these QTLs. Kaiser et al. Nature 2016 Genetic divergence between Port-en-Bessin vs. St Jean populations However, in the circadian-phase C2 QTL (that includes a Tim homolog, tim2), Port-en-Bessin vs. St Jean populations have a high genetic divergence (FST) at the gene encoding calcium2+/Calmodulin kinase II.1. In mice and flies, CaMKII phosphorylates the CLOCK protein. Kaiser et al. Nature 2016  Variability of circadian emergence time maps to CaMKII Different splice forms of CaMKII differ in the length of linker (exon/intron structure shown): RA and RB splice forms of the CaMKII mRNA are differentially expressed in Port-en-Bessin (Por) vs St. Jean (Jean) populations. Does this lead to altered phosphorylation of CLOCK and changes in per/tim transcription ? (not known yet) Kaiser et al. Nature 2016  Conclusion: Clunio circadian/circalunar emergence CamKII polymorphisms correlate with differences in the circadian phase of the semi-lunar/lunar emergence cycle However, we do not know if the CaMKII proteins encoded by the different splice variants differentially phosphorylate CLOCK (or whatever the mechanism might be) Kaiser et al. Nature 2016 Lunar rhythms in the marine annelid Platynereis premature worm mature adults engaged in “mating dance”  Lunar rhythms in the marine annelid Platynereis premature worm mature adults engaged in “mating dance” LD cycle as day/night Maturity rhythm in Platynereis leads to spawning. This rhythm peaks at the new moon (NM) and troughs at the full moon (FM) and free-runs in LD (no light at night as shown). Prior to the freerun in LD, nocturnal dim light is required for ~8 days to entrain/synchronize the population. These data show ~ 131 days. Zantke et al 2013 Cell. Rep. 5, 99-113  LL disrupts the spawning rhythm (left panel)... light during the day light during the night no light during the night... and so does the absence of any moonlight during entrainment (right panel) Zantke et al 2013 Cell. Rep. 5, 99-113 Casein-kinase 1e/d inhibitor (PF-670462) disrupts the circadian locomotor cycle... Zeitgeber time (hour) Zeitgeber time (hour)... and disrupts mRNA daily cycling of Clock and Bmal1 transcripts... Zantke et al 2013 Cell. Rep. 5, 99-113... but leaves lunar spawning rhythm intact This result implies that CK1e/d is not required for lunar cycles but it is for circadian rhythms, suggesting independent mechanism for circadian vs. lunar oscillators Zantke et al 2013 Cell. Rep. 5, 99-113  General Conclusions so far In Eurydice, Clunio, and Platynereis the evidence suggests an independence of the mechanisms underlying circadian and tidal/lunar clocks (although there may be overlapping components). Lunar cycles in Platynereis do not appear to be CK1 dependent whereas tidal rhythms in Eurydice are. In Clunio, QTLs for circadian modulation of semi-lunar/lunar emergence phase include CaMKII (and tim2 but no other canonical clock genes). What about humans and the moon ?  What about humans and the moon ? most intriguing correlation: the lunar cycle and human menstrual cycles (~29.5 days) “Synodic” (lunar) month is the cycle of the full moon & new moon luminance cycle (period = 29.53 days) as the Moon moves through its two points of alignment with the Earth and Sun. The synodic month clearly affects moonlight intensity and gravity (visible in the tides). Helfrich-Förster et al., 2021 What about humans and the moon ? Menstrual cycles of 6 women (birth years in parenthesis) were recorded between 1978 and 2015. Onsets of menses are shown as black dots, while times of full moons (blue lines) and new moons (yellow lines){triple plotted}. Black circles indicate miscarriages; red asterisks indicate births, and triangles indicate gaps in the record. In subjects 1 to 5, the menstrual cycle coupled temporarily to full or new moons. Light blue shaded areas indicate years of Saros #137, which were characterized by high luminance and high gravitational influence of the Moon during periods when Sun-Earth- Moon syzygies coincided with perigees in which the Moon was exceptionally close to Earth. Helfrich-Förster et al., 2021 What about humans and the moon ? Saros #137 Helfrich-Förster et al., 2021  What about humans and the moon ? Menstrual cycle periods of 22 women organized by age younger than 35 y old vs. older than 35 y old Authors’ quote: “With age and upon exposure to artificial nocturnal light, menstrual cycles shortened and lost synchrony with the lunar cycle. We hypothesize that in ancient times, human reproductive behavior was synchronous with the Moon but that our modern lifestyles have changed reproductive physiology and behavior.” Helfrich-Förster et al., 2021  The Moon and Sleep (Werewolf? Full moon? Sleep? Get it?)  The Moon and Sleep (very rural community without access to electricity) Time at which they experience this light intensity Sleep onset/offset Access to electricity is associated with: Later sleep onsets Shorter sleep duration Increased variability in sleep timing between individuals Delayed phase of the circadian clock (you already saw this slide in our 2nd lecture on humans) de la Iglesia et al. (2015) Journal of Biological Rhythms 30: 342–350  The Moon and Sleep Is the time of sleep onset associated with the phase of the moon? Consider the case of sleep duration (A) and sleep onset (B) of the Argentinian Toba/Qom people on the right later onset Casiraghi et al., Sci. Adv. 2021  The Moon and Sleep Human Sleep is Synchronized with the Lunar Cycle Let’s subdivide the entire Toba/Qom community (panels A & B) into three groups (panels C & D): 1. urban setting with full access to electricity (green) 2. rural community with access to limited electric light (orange) 3. rural community with no access to electric light at all (blue) Casiraghi et al., Sci. Adv. 2021  The Moon and Sleep Human Sleep is Synchronized with the Lunar Cycle But it isn’t just true of Argentinian Toba/Qom ! This is a plot of sleep that is synchronized with the moon cycle in Seattle college students !! Qualification : although 464 students (n = 464) were recorded across different academic quarters, there is a lot of variability and the Actiwatch was on their wrists for only 1 to 3 weeks (i.e., less than 1 cycle). {error bars are SEM} Casiraghi et al., Sci. Adv. 2021  The Moon and Sleep Human Sleep is Synchronized with the Lunar Cycle Moonlight...... is associated with a delayed sleep onset and shorter sleep only when available during the first half of the night... is not associated with sleep offset (wake-up) time... has an effect regardless of the level of urbanization... mimics the effects of artificial light ? And vice versa ? Casiraghi et al., Sci. Adv. 2021  The Moon and Sleep Human Sleep is Synchronized with the Lunar Cycle Adaptive value? Hunting & fishing: older men in the Toba/Qom society confirm that men used to take advantage of moonlit nights to fish & hunt Reproductive behavior: interviews from the Toba/Qom society reveal that moonlit nights are times at which young women & men seek each other for sexual encounters. (Mythological stories in different cultures are similar; also note the aforementioned evidence linking the menstrual cycle to the moon) Working hypotheses of these researchers: 1. artificial light has tapped into an ancestral sleep-inhibiting role of moonlight ? 2. The delay in sleep timing of teenagers in industrialized societies could be emulating sleep timing on moonlit nights ? Casiraghi et al., Sci. Adv. 2021  Do you remember this slide from our third “Human Clocks” lecture? Bipolar Disorder: Case Study 2 (1998): Chronotherapy to regularize sleep- wake cycles can be effective in treating bipolar depression in some patients. The patient cycled between depression and mania about every month when he slept according to his usual routine. Could this ~monthly cycling have any thing to do with lunar phase ?? (you already saw this slide in our 3rd lecture on humans) Wehr et al., Biol. Psychiatry 1998  The Moon and Madness aka, Lunacy! (or, are you feeling “loony” yet?) Sleep Duration Full moon 24 h 24.84 h lunar cycles 24.8 h tidal cycle (gravimetric) New moon Left panels: A 35-year-old man with bipolar disorder: after nights of excessive sleep, he was very depressed, while after nights of little sleep, depression lifted, and he had racing thoughts. The timing of his sleep onset shifted progressively earlier each night during the first half of each spring-neap cycle, and progressively later during the second half. Conversely, the timing of his wake onset shifted progressively later each night during the first half of each cycle, and progressively earlier during the second half. Consequently, during the course of each cycle, the duration of sleep shifted back and forth between 0 hours in mania and 12 hours in depression. Nights with little or no sleep regularly coincided with mania & the peaks of the semi-diurnal tidal cycle. Right panels: another example. Avery & Wehr Bipolar Disord. 2018  The Moon and Madness aka, Lunacy! (or, are you feeling “loony” yet?) Drastic reductions in sleep (below) & 24 h switches into mania coincide with transits across the solar day of peaks of every second 14.8 d spring/neap cycle (diagonal lines). 24 h 24.8 h lunar semi-diurnal gravimetric tide Delays in the phase of the BT rhythm (above) & switches into mania coincide with transits across the solar day of peaks of every third 24.8-h tide (red diagonal lines). Wehr, Molecular Psychiatry 2018  Food for Thought Assume for a moment that the mechanisms of the circadian, circatidal, and circalunar clocks are evolutionarily related, i.e., that one mechanism is ancestral and the other mechanisms are a result of gene duplication and then modification of function. (Also, note that there is evidence supporting the hypothesis that the early evolution of life occurred in the ocean; e.g., marine cyanobacteria are possibly the earliest form of life for which we have fossils that date back ~3.5 billion years. In addition, other evidence suggests that early evolution of life–– not necessarily the cyanobacteria––occurred at geothermal vents on the ocean floor.) So... IF the earliest evolution of life occurred in the ocean, which of the three “circa-rhythms” do you think might be ancestral and why? What selective forces might have favored the evolution of the other two “circa-rhythms” from the ancestral one? The data from the menstrual cycles of some women (at some time in their life) and from some BPD patients suggest that at least some humans can (subconsciously) sense & respond to lunar phase. What are they sensing? (i.e., moonlight? gravity?) What do those data imply for the rest of us?