The origin and early evolution of circadian clocks are far from clear. It is now widely believed that the clocks in cyanobacteria and the clocks in Eukarya evolved independently from each other. It is also possible that some Archaea possess clock – at least they have clock genes, thought to have arived there by lateral transfer from cyanobacteria.[continued under the fold]
It is not well known, though, if the clocks in major groups of Eukarya – Protista, Plants, Fungi and Animals – originated independently or out of a common ancestral clock. On one hand, the internal logic of the clock machinery appears to be the same in all Eukarya. It also appears that in all plants, fungi and animals, at least one of the core clock genes has a PAS domain. On the other hand, the identities of clock genes are vastly different between the Kingdoms. Perhaps the last common ancestor possessed something like an hourglass mechanism or even just a simple relay switch, out of which the full-fledged circadian clock evolved independently in different lines of Eukaryotes.
While it is understandable that much of the funding is targeted at medically important research, leading to most chronobiologists working on vertebrates (especially mammals) or the genetics work-horse Drosophila, it is still surprising how little work has been done on the most ancient groups of animals. I could not detect a single study on daily rhythms in Choanoflagellates. There are only a handful of studies in sponges, barely scratching the surface and not even being able to conclude with any degree of certainty if sponges have a clock at all or not.
Now, I turn my attention to Cnidaria. This group has been studied quite intensively lately and recent findings about its development, genetics and phylogenetic relationship to other animals are quite stunning.
While the literature on the daily (and lunar) rhythms in Cnidaria is somewhat larger than that of sponges, it is by no means extensive and most of it suffers form the same weaknesses – studies of rhythms in the field in natural light-dark cycles can detect diurnal rhythms, but cannot determine if those rhythms are also circadian, i.e., if they are generated by an internal endogenous clock.
Let me just briefly refresh your memory on Cnidaria. Those are animals like corals, sea anemones and jellyfish. How, you may ask, do corals and jellyfish get lumped together in one group – after all, they look so different? Cnidaria, as a rule, have a comlex life history cycle. There is a ‘polyp phase’ which is sessile (fixed to the substrate of the ocean floor), it releases gametes which, after fertilization, develop into a larva called ‘planula’. Larva develops into the ‘medusa’ stage which is a freely swimming predator. The medusa can, after a while, drop onto the floor and metamorphose into a polyp again. In many cnidarians, e.g., corals and sea anemones, the polyp phase is dominant – the medusa is small and short-lived. In some, as in Hydra, there is no medusa stage at all. In jellyfish, it is the medusa stage that is dominant – it becomes large and complex and that is what stings you if you are not careful swimming in the ocean. Here, the polyp phase is short and small, or may be abolished altogether.
Many corals have symbionts – zooxanthella. Research on daily rhythms mostly looks at corals or sea anemones in the field, (e.g., B. E. Chalker, D. L. Taylor, Rhythmic Variations in Calcification and Photosynthesis Associated with the Coral Acropora cervicornis (Lamarck), Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 201, No. 1143 (May 5, 1978) , pp. 179-189, or, Boero, F; Cicogna, F; Pessani, D; Pronzato, R, In situ observations on contraction behaviour and diel activity of Halcampoides purpurea var. mediterranea (Cnidaria, Anthozoa) in a marine cave. Marine Ecology. Vol. 12, no. 3, pp. 185-192. 1991.), noting daily changes in movement. Interestingly, melatonin, a hormone apparently ubiqutous in nature and tightly related to visual and circadian physiology, induces movement in sea anemones (WH Tsang, NJ McGaughey, YH Wong, JTY Wong – Melatonin and 5-methoxytryptamine induced muscular contraction in sea anemones – The Journal of Experimental Zoology, 1997, Volume 279, Issue 3, Pages 201 – 207), but there was no attempt to test if melatonin produced its effect directly, or via a circadian mechanism.
In some studies, the rhythms of the coral and its zooxanthela are studied together. For instance, responses of the coral to light, photosynthetic activity of zooxanthela, and biochemical responses of coral to the oxygen produced by zooxanthela all follow the daily cycle and rise and fall with the level of illumination in the ocean (G. Muller-Parker, Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae, Marine Biology, Volume 82, Number 3, pp.225 – 232, September 1984.).
A number of papers notes that release of the larvae is synchronized with the phase of the moon (e.g., P. L. Jokiel, R. Y. Ito and P. M. Liu, Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis, Marine Biology, Volume 88, Number 2, Pages: 167 – 174, August 1985.).
What all of these papers have in common is that there is no attempt to monitor the animals in prolonged constant conditions in order to see if the rhythms persist. Thus, we do not know if the daily rhythms are generated in direct response to daily changes in the environment or if they are generated endogenously by some kind of timer, possibly a proper circadian clock. One exception is this paper – F Sinniger, R Maldonado-Rodriguez, RJ Strasser, Coral life as probed by their fluorescence emission (PDF is protected from copying – click on it to see the figures) – in which photosynthetic driving force in three species of corals kept in the lab in semi-natural conditions exhibited continuous oscillaitons during a four-day period in which the animals were kept in constant darkness. Interestingly, it show three oscillations during that 4-day period. This is sufficient to characterize it as circadian, though. The consensus in the field is that ability to exhibit 2-3 oscillations is sufficient to deem it circadian. If, after that, the rhythms disappear, it is because the circadian clock is a damped oscillator, not because there is no circadian clock at all. This is, to date, the only set of data suggesting that a cnidarian may actually have a true circadian oscillator.
Interestingly, all of those studies were done in the polyp stage of the cnidarian life-cycle. Isn’t it more common-sensical that a freely moving animal would have a clock? Where are the studies in jellyfish? Jellyfish are notoriously difficult to keep in captivity so I doubt that any systematic experiments have been done.
While optic properties of spicules suggest that sponges may be sensitive to light, those animals have no nerve cells. On the other hand, jellyfish have complex nets of neurons and, moreover, they have multitudes of very complex eyes (Nilsson D-E, Gislén L, Coates MM, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201-205.)
Interestingly, though very complex, the jellyfish eyes are not suited for image-detection, e.i., the detection of light radiance. Their lenses are positioned in a way that difuses light. In eyes evolved for vision, the role of the lens is to focus light. So, what are their eyes for? It appears that their eyes are specifically evolved for detection of irradiance – the light intensity – similarly to the melanopsin-containing retinal ganglion cells in mammals, the pineal, parapineal and frontal organ in non-mammalian vertebrates, teh deep brain photoreceptors in non-mammalian vertebrates, and ocelli in arthoropods.
One possibile function for the jellyfish eyes is photokinesis, i.e. perception of light inducing movement, often a very specific type of movement, e.g., swift attack or even swifter retreat (or “freezing” – playing dead). Passing of a shadow over the eyes may mean “shark” or “food” and induce a particular response.
The other possibility is phototaxis, i.e., movement towards (positive phototaxis) or away (negative phototaxis) from light. The main sources of light are the Sun and the Moon. Many aquatic creatures exhibit phototaxis as a way to orient in the vertical column, i.e., light is up, dark is down.
Many aquatic creatures switch their phototaxis between day and night, for instance they may be attracted to light at night (as the food is on the surface) while swimming to the bottom during the day (avoiding UV damage and/or predators).
In order to know when is the day and when is the night, they need to know the time of day, i.e., to have a circadian clock. Another role for the eyes is to entrain the circadian clock to the day/night cycle.
It is possible that there are some aspects of the jellyfish physiology/behavior that are seasonal, e.g., reproduction or migration. Eyes are needed to perceive (and the circadian clock to measure) the changing length of day (photoperiod) and induce appropriate seasonal changes: photoperiodism.
Finally, many aquatic organisms do stuff (e.g., spawn) at a particular phase of the Moon. Light intensity at night is a good (and most relevant) measure of the moon-phase. The eyes may be used to measure the moolight intensity, or, also likely to entrain endogenous circalunar rhythms.
Having two types of eyes with poor focus makes all of the above possible. Real vision (image formation) is the only photoreceptive function that is excluded.
In vertebrates like us, such eyes (that little subset of retinal ganglion cells I mentioned above) have additional functions, e.g., pupilar reflex (pupils get smaller in brighter light), melatonin secretion (bright light quickly and severely shuts down melatonin synthesis in the eyes and the pineal) and control of mood (the axons project directly to the “mood center” in the brain, explaining to some extent the depression-inducing effects of prolonged darkness, e.g., in prisons).
A recent article describes a cool radiotelemetry experiment with jellyfish in the field. The animals were active during the day and inactive during the night. A flash of light temporarily activated them during the night, but the response was short-lived: Seymour J, Carrette T, & Sutherland P. 2004. Do box jellyfish sleep at night?. Medical Journal of Australia 181: 707.. I hope that the studies continue. Knowing if cnidarians have circadian clocks, what genes they use (and how) to run the clock, and what adaptive functions their clocks may have, would illuminate the quesiton of origin and early evolution of animal circadian rhythms and clocks.