Skip to main content
SpringerLink
Log in

Local Adaptations of Circalunar and Circadian Clocks: The Case of Clunio marinus

  • Chapter
  • First Online:
Annual, Lunar, and Tidal Clocks

Abstract

Biological clocks are considered to increase an organism’s fitness in that they allow the synchronization of reproduction, physiology, and behavior with environmental conditions. Indirect evidence for the biological fitness value comes from the existence of local timing adaptations within a species. Some of the most clear cut examples of adaptations in circalunar and circadian clocks are found in the intertidal midge Clunio marinus. In adaptation to the local tidal regime, populations of this insect differ in the phase of the circadian clock, as well as in the phase, period, and zeitgeber sensitivity of the circalunar clock. These differences allow comparative genetic and molecular studies that may both shed light on the evolutionary forces shaping biological clocks and unravel the first known molecular components of a circalunar clock.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abbot P, Withgott JH (2004) Phylogenetic and molecular evidence for allochronic speciation in gall-forming aphids (Pemphigus). Evolution 58(3):539–553

    Article  CAS  PubMed  Google Scholar 

  • Alexander RD, Bigelow RS (1960) Allochronic speciation in field crickets, and a new species, Acheta veletis. Evolution 14(3):334–346

    Article  Google Scholar 

  • Christy JH (1978) Adaptive significance of reproductive cycles in the fiddler crab Uca pugilator: a hypothesis. Science 199(4327):453–455

    Article  CAS  PubMed  Google Scholar 

  • Corbet PS (1958) Lunar periodicity of aquatic insects in Lake Victoria. Nature (Lond) 182(4631):330–331

    Article  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309(5734):630–633

    Article  CAS  PubMed  Google Scholar 

  • Endraß U (1976) Physiological adaptations of a marine insect. 2. Characteristics of swimming and sinking egg-masses. Mar Biol 36(1):47–60

    Article  Google Scholar 

  • Enright JT (1972) Virtuoso isopod: circa-lunar rhythms and their tidal fine-structure. J Comp Physiol 77(2):141–162

    Article  Google Scholar 

  • Filchak KE, Roethele JB, Feder JL (2000) Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature (Lond) 407(6805):739–742

    Article  CAS  Google Scholar 

  • Foster SA (1987) Diel and lunar patterns of reproduction in the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and Abudefduf troschelii. Mar Biol 95(3):333–343

    Article  Google Scholar 

  • Franke H-D (1985) On a clocklike mechanism timing lunar-rhythmic reproduction in Typosyllis prolifera (Polychaeta). J Comp Physiol Sens Neural Behav Physiol 156(4):553–561

    Google Scholar 

  • Futuyma DJ (2009) Evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL (1984) Mass spawning in tropical reef corals. Science 223(4641):1186–1189

    Article  CAS  PubMed  Google Scholar 

  • Hartland-Rowe R (1955) Lunar rhythm in the emergence of an ephemeropteran. Nature (Lond) 176:657

    Article  Google Scholar 

  • Hauenschild C (1960) Lunar periodicity. Cold Spring Harbor Symp Quant Biol 25:491–497

    Article  CAS  PubMed  Google Scholar 

  • Hauenschild C, Fischer A, Hofmann DK (1968) Untersuchungen am pazifischen Palolowurm Eunice viridis (Polychaeta) in Samoa. Helgol Wiss Meeres 18(3):254–295

    Google Scholar 

  • Heimbach F (1976) Semilunare und diurnale Schlüpfrhythmen südenglischer und norwegischer Clunio-Populationen (Diptera, Chironomidae). Ph.D. thesis, Universität Köln, Köln

    Google Scholar 

  • Heimbach F (1978) Sympatric species, Clunio marinus Hal. and Cl. balticus n. sp. (Dipt., Chironomidae), isolated by differences in diel emergence time. Oecologia (Berl) 32(2):195–202

    Article  Google Scholar 

  • Hofmann W, Winn K (2000) The littorina transgression in the Western Baltic Sea as indicated by subfossil Chironomidae (Diptera) and Cladocera (Crustacea). Int Rev Hydrobiol 85(2-3):267–291

    Article  Google Scholar 

  • Kaiser TS, Heckel DG (2012) Genetic architecture of local adaptation in lunar and diurnal emergence times of the marine midge Clunio marinus (Chironomidae, Diptera). PLoS One 7(2):e32092

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaiser TS, Neumann D, Heckel DG, Berendonk TU (2010) Strong genetic differentiation and postglacial origin of populations in the marine midge Clunio marinus (Chironomidae, Diptera). Mol Ecol 19(14):2845–2857

    Article  CAS  PubMed  Google Scholar 

  • Kaiser TS, Neumann D, Heckel DG (2011) Timing the tides: genetic control of diurnal and lunar emergence times is correlated in the marine midge Clunio marinus. BMC Genet 12:49

    Article  PubMed Central  PubMed  Google Scholar 

  • Klapow LA (1972) Fortnightly molting and reproductive cycles in sand-beach isopod, Excirolana chiltoni. Biol Bull 143(3):568–591

    Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Kronfeld-Schor N, Dominoni D, de la Iglesia H, Levy O, Herzog ED, Dayan T, Helfrich-Forster C (2013) Chronobiology by moonlight. Proc R Soc B Biol Sci 280(1765)

    Google Scholar 

  • Lessios HA (1984) Possible prezygotic reproductive isolation in sea-urchins separated by the Isthmus of Panama. Evolution 38(5):1144–1148

    Article  Google Scholar 

  • Levin DA (1978) The origin of isolating mechanisms in flowering plants. In: Hecht MK, Steere WC, Wallace B (eds) Evolutionary biology, vol 11. Plenum Press, New York, pp 185–317

    Chapter  Google Scholar 

  • Lloyd JE (1966) Studies on the flash communication system in Photinus fireflies. Misc Publ Mus Zool Univ Mich 130:1–95

    Google Scholar 

  • Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist. Columbia biological series, vol 13. Columbia University Press, New York

    Google Scholar 

  • Mayr E (1970) Populations, species, and evolution: an abridgement of animal species and evolution. Belknap Press, Cambridge

    Google Scholar 

  • Michailova P (1980) A review of the European species of genus Clunio Haliday, 1855 (Diptera, Chronomidae). Zool Anz 205(5-6):417–432

    Google Scholar 

  • Muthiga NA (2003) Coexistence and reproductive isolation of the sympatric echinoids Diadema savignyi Michelin and Diadema setosum (Leske) on Kenyan coral reefs. Mar Biol 143(4):669–677

    Article  Google Scholar 

  • Naylor E (1989) Temporal aspects of adaptation in the behavioural physiology of marine animals. In: 21st European marine biology symposium. Polish Academy of Sciences, Gdansk, pp 123–135

    Google Scholar 

  • Naylor E (2001) Marine animal behaviour in relation to lunar phase. Earth Moon Planets 85-86:291–302

    Article  Google Scholar 

  • Neumann D (1966) Die lunare und tägliche Schlüpfperiodik der Mücke Clunio: Steuerung und Abstimmung auf die Gezeitenperiodik. Z Vgl Physiol 53(1):1–61

    Google Scholar 

  • Neumann D (1967) Genetic adaptation in emergence time of Clunio populations to different tidal conditions. Helgol Wiss Meeres 15(1-4):163–171

    Article  Google Scholar 

  • Neumann D (1983) Die zeitliche Programmierung von Tieren auf periodische Umweltbedingungen. Rhein-Westfael Akad Wiss Nat- Ing- Wirtschwiss 324:31–62

    Google Scholar 

  • Neumann D (1986) Life cycle strategies of an intertidal midge between subtropic and arctic latitudes. In: Taylor F, Karban R (eds) The evolution of insect life cycles. Springer, New York, pp 3–19

    Chapter  Google Scholar 

  • Neumann D (1989) Circadian components of semilunar and lunar timing mechanisms. J Biol Rhythms 4(2):285–294

    Article  CAS  PubMed  Google Scholar 

  • Neumann D (1995) Physiologische Uhren von Insekten: zur Ökophysiologie lunarperiodisch kontrollierter Fortpflanzungszeiten. Naturwissenschaften 82(7):310–320

    Article  Google Scholar 

  • Neumann D, Heimbach F (1979) Time cues for semilunar reproduction rhythms in European populations of Clunio marinus. I. The influence of tidal cycles of mechanical disturbance. In: Naylor E, Hartnoll RG (eds) Cyclic phenomena in marine plants and animals. Pergamon Press, Oxford, pp 423–433

    Chapter  Google Scholar 

  • Neumann D, Heimbach F (1984) Time cues for semilunar reproduction rhythms in European populations of Clunio marinus. 2. The influence of tidal temperature cycles. Biol Bull 166(3):509–524

    Article  Google Scholar 

  • O’Donnell AJ, Schneider P, McWatters HG, Reece SE (2011) Fitness costs of disrupting circadian rhythms in malaria parasites. Proc R Soc B Biol Sci 278(1717):2429–2436

    Article  Google Scholar 

  • Oka H, Hashimoto H (1959) Lunar periodicity in the propagation of a Pacific species of Clunio (Diptera, Chironomidae). Biol Zentralbl 78(4):545–559

    Google Scholar 

  • Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in Cyanobacteria. Proc Natl Acad Sci USA 95(15):8660–8664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palstra AP, De Graaf M, Sibbing FA (2004) Riverine spawning and reproductive segregation in a lacustrine cyprinid species flock, facilitated by homing? Anim Biol 54(4):393–415

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Pearse JS (1990) Lunar reproductive rhythms in marine invertebrates: maximizing fertilization? Adv Invertebr Reprod 5:311–316

    Google Scholar 

  • Reid DG, Naylor E (1985) Free-running, endogenous semilunar rhythmicity in a marine isopod crustacean. J Mar Biol Assoc UK 65(1):85–91

    Article  Google Scholar 

  • Reid DG, Naylor E (1986) an entrainment model for semilunar rhythmic swimming behavior in the marine isopod Eurydice pulchra Leach. J Exp Mar Biol Ecol 100(1–3):25–35

    Article  Google Scholar 

  • Saigusa M (1980) Entrainment of a semilunar rhythm by a simulated moonlight cycle in the terrestrial crab, Sesarma haematocheir. Oecologia (Berl) 46(1):38–44

    Article  Google Scholar 

  • Saigusa M (1986) The circa-tidal rhythm of larval release in the incubating crab Sesarma. J Comp Physiol Sens Neural Behav Physiol 159(1):21–31

    Article  Google Scholar 

  • Saigusa M, Akiyama T (1995) The tidal rhythm of emergence, and the seasonal variation of this synchrony, in an intertidal midge. Biol Bull 188(2):166–178

    Article  Google Scholar 

  • Saunders DS (1972) Circadian control of larval growth rate in Sarcophaga argyrostoma. Proc Natl Acad Sci USA 69(9):2738–2740

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith DC (1988) Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature (Lond) 336(6194):66–67

    Article  Google Scholar 

  • Soong K, Leu Y (2005) Adaptive mechanism of the bimodal emergence dates in the intertidal midge Pontomyia oceana. Mar Ecol Prog Ser 286:107–114

    Article  Google Scholar 

  • Soong KY, Chen JY, Tsao CJ (2006) Adaptation for accuracy or for precision? Diel emergence timing of the intertidal insect Pontomyia oceana (Chironomidae). Mar Biol 150(2):173–181

    Article  Google Scholar 

  • Tauber CA, Tauber MJ (1977) Sympatric speciation based on allelic changes at three loci: evidence from natural populations in two habitats. Science 197(4310):1298–1299

    Article  CAS  PubMed  Google Scholar 

  • Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP (2003) Temporal mating isolation driven by a behavioral gene in Drosophila. Curr Biol 13(2):140–145

    Article  CAS  PubMed  Google Scholar 

  • Yerushalmi S, Green RM (2009) Evidence for the adaptive significance of circadian rhythms. Ecol Lett 12(9):970–981

    Article  PubMed  Google Scholar 

  • Zantke J, Ishikawa-Fujiwara T, Arboleda E, Lohs C, Schipany K, Hallay N, Straw AD, Todo T, Tessmar-Raible K (2013) Circadian and circalunar clock interactions in a marine annelid. Cell Rep 5(1):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(19):1863–1873

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Max F. Perutz Laboratories, Wien, Austria

    Tobias S. Kaiser

Authors
  1. Tobias S. Kaiser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tobias S. Kaiser .

Editor information

Editors and Affiliations

  1. Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, Japan

    Hideharu Numata

  2. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom

    Barbara Helm

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Japan

About this chapter

Cite this chapter

Kaiser, T.S. (2014). Local Adaptations of Circalunar and Circadian Clocks: The Case of Clunio marinus . In: Numata, H., Helm, B. (eds) Annual, Lunar, and Tidal Clocks. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55261-1_7

Download citation

Publish with us

Policies and ethics

Search

Navigation