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The Clock-Work Worms: Diversity and Function of Clock Expression in Marine Polychaete Worms

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Abstract

Polychaetes are marine worms that display a surprising array of reproductive modes that are usually highly synchronized to the complex cycles of the marine environment. From the extremely long metonic (19-year) cycles of reproduction in the Palolo worm to the short ultradian tidal (12.4 h) cycles of feeding in the ragworm, polychaetes demonstrate a great diversity of entrainment to all known environmental cycles in the oceans. They are able to tell the time of the year, month, day, and tide and hence they may be considered the ultimate marine chronometers, a trait that is under strong selection pressure, ultimately increasing fitness. Polychaetes evolved before the great Cambrian explosion 600 million years ago, and hence it seems probable that their clock phenotypes and genotypes constitute the ancestral protoclock that either predates, or at least coevolved with, the circadian time piece we know so much about today.

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References

  • Aldrich JC (1997) Crab clocks sent for recalibration. Chronobiol Int 14:435–437

    Article  CAS  PubMed  Google Scholar 

  • Barnwell FH (1966) Daily and tidal patterns of activity in individual fiddler crabs from the Woods Hole region. Biol Bull 130:1–17

    Article  CAS  PubMed  Google Scholar 

  • Benn C (2001) The moon and the origin of life. Earth Moon Planets 85–86:61–66

    Google Scholar 

  • Bentley MG, Pacey AA (1992) Physiological and environmental control of reproduction in polychaetes. Oceanogr Mar Biol Annu Rev 30:443–481

    Google Scholar 

  • Boeing WJ, Leech DM, Williamson CE, Cooke S, Torres L (2004) Damaging UV radiation and invertebrate predation: conflicting selective pressures for zooplankton vertical distribution in the water column of low DOC lakes. Oecologia (Berl) 138:603–612

    Article  Google Scholar 

  • Bollens SM, Frost BW, Thoreson DS, Watts SJ (1992) Diel vertical migration in zooplankton: field evidence in support of the predator avoidance hypothesis. Hydrobiologia 234:33–39

    Article  Google Scholar 

  • Bünning E (1936) Die endogene Tagesrhythmik als Grundlage der Photoperiodischen Reaction. Ber Dtsch Bot Ges 54:590–607

    Google Scholar 

  • Carter CG, Grove DJ, Carter DM (1991) Trophic resource partitioning between two coexisting flatfish species off the north coast of Anglesey, North Wales. Neth J Sea Res 23:325–335

    Article  Google Scholar 

  • Caspers H (1961) Beobachtung über Lebensraum and Schwamperiodizität des Palolowurmes Eunice viridis. Int Rev Ges Hydriobiol 46:175–183

    Article  Google Scholar 

  • Chu JW, Levin LA (1989) Photoperiod and temperature regulation of growth and reproduction in Streblospio benedicti (Polychaeta: Spionidae). Invertebr Reprod Dev 15:131–142

    Article  Google Scholar 

  • Clark S (1987) Long term biological rhythmicity and reproduction: an experimental study of Harmothoe imbicata (L.) (Polychaeta: Polynoidae). Ph.D. thesis, University of Newcastle, Newcastle upon Tyne

    Google Scholar 

  • Clark S (1988) A two phase photoperiodic response controlling the annual gametogenic cycle in Harmothoe imbricate (L.). Invertebr Reprod Dev 14:245–266

    Article  Google Scholar 

  • Enright JT (1976) Resetting a tidal clock: a phase-response curve for Excirolana. In: DeCoursey DJ (ed) Biological rhythms in the marine environment. University of South Carolina Press, Columbia, pp 103–114

    Google Scholar 

  • Fischer A (1965) Über Die Chromatophoren und den farbwechsel bei dem Polychaten Platyenereis dumerilii. Z Zellforsch Mikr Anat 65:290–312

    CAS  Google Scholar 

  • Fischer A, Dorresteijn A (2004) The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. Bioessays 26:314–325

    Article  PubMed  Google Scholar 

  • Fong PP (1993) Lunar control of epitokal swarming in the polychaete Platynereis bicanaliculata (Baird) from Central California. Bull Mar Sci 52:911–924

    Google Scholar 

  • Fong PP, Pearse JS (1992a) Photoperiodic regulation of parturition in the self fertilising viviparous polychaete Neanthes limnicola from central California. Mar Biol 112:81–89

    Article  Google Scholar 

  • Fong PP, Pearse JS (1992b) Evidence for a programmed circannual life-cycle modulated by increasing daylengths in Neanthes limnicola (Polychaeta: Nereidae) from central California. Biol Bull 182:289–297

    Article  Google Scholar 

  • Franke HD (1985) On a clocklike mechanism timing lunar-rhythmic reproduction in Typosyllis prolifera (Polychaeta). J Comp Physiol A 156:553–561

    Article  Google Scholar 

  • Franke HD (1986a) The role of light and other endogenous factors in the timing of the reproductive cycle of Typosyllis prolifera and some other polychaetes. Am Zool 26:433–445

    Google Scholar 

  • Franke HD (1986b) Resetting a circalunar reproduction rhythm with artificial moonlight signals: phase-response curve and ‘moon-off’ effect. J Comp Physiol A 159:569–576

    Article  Google Scholar 

  • Fuller CM, Butman CA, Conway NM (1988) Periodicity in fecal pellet production by the capitellid polychaete Mediomastus ambiseta throughout the day. Ophelia 29:83–91

    Article  Google Scholar 

  • Garwood PR (1980) The role of temperature and daylength in the control of the reproductive cycle of Harmathoe imbricata (L.) (Polychaeta: Polynoidae). J Exp Mar Biol Ecol 47:35–53

    Article  Google Scholar 

  • Garwood PR (1981) Observations on the cytology of the developing female germ-cell in the polychaete Harmothoe imbricata (L). Int J Invertebr Reprod 3:333–345

    Article  Google Scholar 

  • Garwood PR, Olive PJW (1978) Environmental control of reproduction in the polychaetes Eulalia viridis and Harmothoe imbricata. In: McLusky DS, Berry AJ (eds) 12th European symposium on marine biology, vol 1. Pergamon Press, Stirling, pp 321–339

    Google Scholar 

  • Garwood PR, Olive PJW (1982) The influence of photoperiod on oocyte growth and its role in the control of the reproductive cycle of the polychaete Harmothoe imbricata (L.). Int J Invertebr Reprod 5:161–165

    Article  Google Scholar 

  • Gray J (1847) An account of Palolo, a sea worm eaten in the Navigator Islands. Proc Zool Soc Lond 15:17–18

    Google Scholar 

  • Hardege JD, Muller CT, Beckman M, Bartels Hardege HD, Bentley MG (1998) Timing of reproduction in marine polychaetes: the role of sex pheromones. Ecoscience 5:395–404

    Google Scholar 

  • Hauenschild C, Fischer A, Hofmann DK (1968) Untersuchungen am pacifischen Palolowurm Eunice viridis (Polychaeta) in Samoa. Helgoland Wiss Meer 18:254–295

    Article  Google Scholar 

  • Krasinsky G (2002) Dynamical history of the Earth–Moon system. Celest Mech Dyn Astr 84:27–55

    Article  Google Scholar 

  • Last KS (2000) Photoperiodism in the semelparous polychaete Nereis virens sars. PhD thesis. University of Newcastle upon Tyne

    Google Scholar 

  • Last KS (2003) An actograph and its use in the study of foraging behaviour in the benthic polychaete, Nereis virens Sars. J Exp Mar Biol Ecol 287:237–248

    Article  Google Scholar 

  • Last KS, Olive PJW (1999) Photoperiodic control of growth and segment proliferation by Nereis (Neanthes) virens Sars in relation to real time and state of maturity. Mar Biol 134:191–200

    Article  Google Scholar 

  • Last KS, Olive PJW (2004) Interaction between photoperiod and an endogenous seasonal factor in influencing the diel locomotor activity of the benthic polychaete Nereis virens Sars. Biol Bull 206:103–112

    Article  PubMed  Google Scholar 

  • Last K, Olive PJW, Edwards A (1999) An actographic study of diel activity in the semelparous polychaete Nereis (Neanthes) virens Sars in relation to the annual cycle of growth. Invertebr Reprod Dev 35:141–145

    Article  Google Scholar 

  • Last KS, Bailhache T, Kramer C, Kyriacou CP, Rosato E, Olive PJ (2009) Tidal, daily, and lunar-day activity cycles in the marine polychaete Nereis virens. Chronobiol Int 26:167–183

    Article  PubMed  Google Scholar 

  • Lewbart GA, Riser NW (1996) Nuchal organs of the polychaete Parapionosyllis manca (Syllidae). Invertebr Biol 115:286–298

    Article  Google Scholar 

  • Lillie FR, Just EE (1913) Breeding habits of the heteronereis form of Nereis limbata at Woods Hole, Mass. Biol Bull 24:147–168

    Google Scholar 

  • Mat AM, Massabuau J-C, Ciret P, Tran D (2012) Evidence for a plastic dual circadian rhythm in the oyster Crassostrea gigas. Chronobiol Int 29:857–867

    Article  PubMed  Google Scholar 

  • Mat A, Massabuau J-C, Ciret P, Tran D (2013) Looking for the clock mechanism responsible for circatidal behavior in the oyster Crassostrea gigas. Mar Biol 1–11

    Google Scholar 

  • Naylor E (1996) Crab clockwork: the case for interactive circatidal and circadian oscillators controlling rhythmic locomotor activity of Carcinus maenas. Chronobiol Int 13:153–161

    Article  CAS  PubMed  Google Scholar 

  • Naylor E (2001) Marine animal behaviour in relation to lunar phase. Earth Moon and Planets 85-6: 291–302

    Google Scholar 

  • Naylor E (2010) Chronobiology of marine organisms. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Naylor E, Atkinson R (1976) Rhythmic behaviour of nephrops and some other marine crustaceans. In: Spencer Davies P (ed) Perspectives in experimental biology, vol 1, Zoology. Pergamon Press, Oxford, pp 135–143

    Google Scholar 

  • Naylor E, Rejeki S (1996) Tidal migrations and rhythmic behaviour of sandbeach crustacea. Rev Chil Hist Nat 69:475–484

    Google Scholar 

  • Neumann D, Heimbach F (1985) Circadian range of entrainment in the semilunar eclosion rhythm of the marine insect Clunio marinus. J Insect Physiol 31:549–557

    Article  Google Scholar 

  • Olive PJW (1971) Ovary structure and oogenesis in Cirratulus cirratus (Polychaeta: Cirratulidae). Mar Biol 8:243–260

    Article  Google Scholar 

  • Olive PJW (1973) The regulation of ovary function in Cirratulus cirratus (Polychaeta). Gen Comp Endocrinol 20:1–15

    Article  CAS  PubMed  Google Scholar 

  • Olive PJW (1980) Control of the reproductive cycle in female Eulalia viridis (Polychaeta: Phyllodocidae). J Mar Biol Assoc UK 61:941–958

    Article  Google Scholar 

  • Olive PJW (1984) Environmental control of reproduction in Polychaeta. Fortschr Zool 29:17–38

    Google Scholar 

  • Olive PJW (1995) Annual breeding cycles in marine invertebrates and environmental temperature: probing the proximate and ultimate causes of reproductive synchrony. J Therm Biol 20:79–90

    Article  Google Scholar 

  • Olive PJW, Garwood PR (1983) The importance of long term endogenous rhythms in the maintenance of reproductive cycles of marine invertebrates: a reappraisal. Int J Invertebr Reprod 6:339–347

    Article  Google Scholar 

  • Olive PJW, Pillai G (1983) Reproductive biology of the polychaete Kefersteinia cirrata Keferstein (Hesionidae). 1. Ovary structure and oogenesis. Int J Invertebr Reprod 6:295–306

    Article  Google Scholar 

  • Olive PJW, Fletcher J, Rees S, Desrosiers G (1997) Interactions of environmental temperature with photoperiod in determining age at maturity in a semelparous polychaete Nereis (Neanthes) virens Sars. J Therm Biol 22:489–497

    Article  Google Scholar 

  • Olive PJW, Kyriacou CP, Last KS, Kramer CAS, Bailhache T, Rosato E (2005) Dancing to the rhythms of geological time: the biorhythm capabilities of Polychaeta in a geological context. Invertebr Reprod Dev 48:197–206

    Article  Google Scholar 

  • Palmer JD (1974) Biological clocks in marine organisms. Wiley, New York

    Google Scholar 

  • Palmer JD (1995a) Review of the dual-clock control of tidal rhythms and the hypothesis that the same clock governs both circatidal and circadian rhythms. Chronobiol Int 12:299–310

    Article  Google Scholar 

  • Palmer JD (1995b) The biological rhythms and clocks of intertidal animals. Oxford University Press, New York

    Google Scholar 

  • Palmer JD (1997) Dueling hypotheses: circatidal versus circalunidian battle basics. Chronobiol Int 14:337–346

    Article  CAS  PubMed  Google Scholar 

  • Palmer JD, Round FE (1967) Persistent vertical migration rhythms in benthic microflora. 6. The tidal and diurnal nature of the rhythm in the diatom Hantzschia virgata. Biol Bull 132:44–55

    Article  Google Scholar 

  • Palmer JD, Williams BG (1986) Comparative studies of tidal rhythms. II. The dual clock control of the locomotor rhythms of two decapod crustaceans. Mar Behav Physiol 12:269–278

    Article  Google Scholar 

  • Peterson KJ (2001) Fossils, molecular clocks and the Cambrian explosion. GSA Annual Meeting, November 5–8, 2001. https://gsa.confex.com/gsa/2001AM/finalprogram/abstract_26837.htm

  • Peterson KJ, Lyons JB, Nowak KS, Takacs CM, Wargo MJ, McPeek MA (2004) Estimating metazoan divergence times with a molecular clock. Proc Natl Acad Sci USA 101:6536–6541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reid DG, Naylor E (1988) Multiple oscillator control of circatidal rhythmicity in the shore crab Carcinus maenas. J Interdiscipl Cycle Res 19:205

    Google Scholar 

  • Riisgard HU, Vedel A, Boye H, Larsen PS (1992) Filter-net structure and pumping activity in the polychaete Nereis diversicolor: effects of temperature and pump modeling. Mar Ecol Prog Ser 83:79–89

    Article  Google Scholar 

  • Saigusa M (1992) Phase shift of a tidal rhythm by light dark cycles in the semiterrestrial crab Sesarma pictum. Biol Bull 182:257–264

    Article  Google Scholar 

  • Saigusa M, Oishi K (2000) Emergence rhythms of subtidal small invertebrates in the subtropical sea: nocturnal patterns and variety in the synchrony with tidal and lunar cycles. Zool Sci 17:241–251

    Article  Google Scholar 

  • Saunders DS, Bertossa RC (2011) Deciphering time measurement: the role of circadian ‘clock’ genes and formal experimentation in insect photoperiodism. J Insect Physiol 57:557–566

    Article  CAS  PubMed  Google Scholar 

  • Schaum E, Last KS, Batty RS (2013) Smelling danger: alarm cue responses in the polychaete worm Nereis diversicolor (Müller, 1776) to fish. PLoS One 8:e77431

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schieges KL (1979) Field and laboratory investigations of factors controlling schizogamous reproduction in the polychaete, Autolytus. Int J Invertebr Reprod 1:359–370

    Article  Google Scholar 

  • Schroeder PC, Hermans CO (1975) Annelida: polychaeta. In: Geise AC, Pearse JS (eds) Reproduction of marine invertebrates, vol 3. Academic, New York, pp 1–213

    Chapter  Google Scholar 

  • Scott DM, Mazurkiewicz M, Leeman P (1976) The long-term monitoring of ventilation rhythms of the polychaetous annelid Nereis virens Sars. Comp Biochem Physiol A 53:65–68

    Article  CAS  PubMed  Google Scholar 

  • Tauber E, Last KS, Olive PJW, Kyriacou CP (2004) Clock gene evolution and functional divergence. J Biol Rhythms 19:445–458

    Article  CAS  PubMed  Google Scholar 

  • Tessmar-Raible K, Raible F, Arboleda E (2011) Another place, another timer: marine species and the rhythms of life. Bioessays 33:165–172

    Article  PubMed Central  PubMed  Google Scholar 

  • Thijssen R, Lever AJ, Lever J (1974) Food composition and feeding periodicity of 0-group plaice (Pleuronectes platessa) in the tidal area of a sandy beach. Neth J Sea Res 8:369–377

    Article  Google Scholar 

  • Tran D, Nadau A, Durrieu G, Ciret P, Parisot J-P, Massabuau J-C (2011) Field chronobiology of a molluscan bivalve: how the moon and sun cycles interact to drive oyster activity rhythms. Chronobiol Int 28:307–317

    Article  PubMed  Google Scholar 

  • Watson GJ, Hamilton KM, Tuffnail WE (2005) Chemical alarm signalling in the polychaete Nereis (Neanthes) virens (Sars) (Annelida: Polychaeta). Anim Behav 70:1125–1132

    Article  Google Scholar 

  • Webb HM (1971) In living organisms: animals. J Interdiscipl Cycle Res 2:191–198

    Article  Google Scholar 

  • Wilson WH (1991a) The foraging ecology of migratory shorebirds in marine soft sediment communities: the effects of episodic predation on prey populations. Am Zool 31:840–848

    Google Scholar 

  • Wilson WH (1991b) The importance of epibenthic predation and ice disturbance in a Bay of Fundy mudflat. Ophelia Suppl 5:507–514

    Google Scholar 

  • Zantke J, Ishikawa-Fujiwara T, Arboleda E, Lohs C, Schipany K, Hallay N, Straw AD, Tessmar-Raible K (2013) Circadian and circalunar clock interactions in a marine annelid. Cell Rep 5:99–113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang L, Hastings MH, Green EW, Tauber E, Sladek M, Webster SG, Kyriacou CP, Wilcockson DC (2013) Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra. Curr Biol 23:1863–1873

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Last, K.S., Hendrick, V.J. (2014). The Clock-Work Worms: Diversity and Function of Clock Expression in Marine Polychaete Worms. In: Numata, H., Helm, B. (eds) Annual, Lunar, and Tidal Clocks. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55261-1_10

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