Timing the tides: Genetic control of diurnal and lunar emergence times is correlated in the marine midge Clunio marinus

BMC Genetics

Volumn 12, Issue , 2011, Pages

  Kaiser, Tobias S ^a,b   Neumann, Dietrich ^c   Heckel, David G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b MAX F PERUTZ LABORATORIES   (Austria)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACKCROSSING; CIRCADIAN RHYTHM; CLUNIO MARINUS; CONTROLLED STUDY; DIURNAL EMERGENCE TIME; EVOLUTIONARY ADAPTATION; GENETIC CORRELATION; GENETIC CROSS; GENETIC REGULATION; GENETIC STRAIN; LUNAR EMERGENCE TIME; LUNAR RHYTHM; MARINE SPECIES; MULTIFACTORIAL INHERITANCE; NATURAL POPULATION; NONHUMAN; PHENOTYPE; PHOTOPERIODICITY; TIDE; TIME; ADAPTATION; ANIMAL; CHIRONOMIDAE; CROSS BREEDING; ENVIRONMENT; GENETIC LINKAGE; GENETICS; LIGHT; MOLECULAR EVOLUTION; MOON; PHYSIOLOGY; PLEIOTROPY; TSUNAMI;

CHIRONOMIDAE; CLUNIO MARINUS; DIPTERA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CHIRONOMIDAE; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CROSSES, GENETIC; ENVIRONMENT; EVOLUTION, MOLECULAR; GENETIC LINKAGE; GENETIC PLEIOTROPY; LIGHT; MOON; TIDAL WAVES; TIME FACTORS;

EID: 79956191255     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-12-49     Document Type: Article

References (53)

1. Franke HD. The role of light and endogenous factors in the timing of the reproductive-cycle of Typosyllis prolifera and some other polychaetes. American Zoologist 1986, 26(2):433-445.
2. Hauenschild C. Lunar Periodicity. Cold Spring Harbor Symposia on Quantitative Biology 1960, 25:491-497.
3. Neumann D. Die lunare und tägliche Schlüpfperiodik der Mücke Clunio - Steuerung und Abstimmung auf die Gezeitenperiodik. Zeitschrift für Vergleichende Physiologie 1966, 53(1):1-61. 10.1007/BF00343045, 19349661.
4. Saigusa M. Entrainment of a Semilunar Rhythm by a Simulated Moonlight Cycle in the Terrestrial Crab, Sesarma haematocheir. Oecologia 1980, 46(1):38-44.
5. Naylor E. Marine animal behaviour in relation to lunar phase. Earth Moon and Planets 2001, 85-6:291-302.
6. Korringa P. Lunar Periodicity. Memoirs of the Geological Society of America 1957, 67:917-934.
7. Neumann D. Tidal and Lunar Rhythms. Handbook of Behavioural Neurobiology 1981, 4:351-380. New York and London: Plenum Publishing Corporation, Aschoff J.
8. Christy JH. Adaptive Significance of Reproductive Cycles in the Fiddler Crab Uca pugilator - A Hypothesis. Science 1978, 199(4327):453-455. 10.1126/science.199.4327.453, 17820580.
9. Caspers H. Spawning Periodicity and Habitat of the Palolo Worm Eunice Viridis (Polychaeta, Eunicidae) in the Samoan Islands. Marine Biology 1984, 79(3):229-236.
10. Hauenschild C, Fischer A, Hofmann DK. Investigations on Pacific Paloloworm Eunice Viridis (Polychaeta) in Samoa. Helgoländer Wissenschaftliche Meeresuntersuchungen 1968, 18(3):254-295.
11. Fryer G. Lunar cycles in lake plankton. Nature 1986, 322:306.
12. Corbet PS. Lunar Periodicity of Aquatic Insects in Lake Victoria. Nature 1958, 182(4631):330-331.
13. Knowlton N. Sibling Species in the Sea. Annual Review of Ecology and Systematics 1993, 24:189-216.
14. Palumbi SR. Genetic Divergence, Reproductive Isolation, and Marine Speciation. Annual Review of Ecology and Systematics 1994, 25:547-572.
15. Hendry AP, Day T. Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecology 2005, 14(4):901-916. 10.1111/j.1365-294X.2005.02480.x, 15773924.
16. DeCoursey PJ. Egg-hatching rhythms in three species of fiddler crabs. European Marine Biology Symposium 1979, 399-406.
17. Enright JT. Virtuoso Isopod - Circa-Lunar Rhythms and Their Tidal Fine-Structure. Journal of Comparative Physiology 1972, 77(2):141-162.
18. Klapow LA. Fortnightly molting and reproductive-cycles in sand-beach isopod, Excirolana chiltoni. Biological Bulletin 1972, 143(3):568-591.
19. Reid DG, Naylor E. Free-Running, Endogenous Semilunar Rhythmicity in a Marine Isopod Crustacean. Journal of the Marine Biological Association of the United Kingdom 1985, 65(1):85-91.
20. Williams JA. A semi-lunar rhythm of locomotor activity and moult synchrony in the sand-beach amphipod Talitrus saltator. European Marine Biology Symposium 1979, 407-414.
21. Hsiao SM, Meier AH. Freerunning circasemilunar spawning rhythm of Fundulus grandis and its temperature compensation. Fish Physiology and Biochemistry 1992, 10(3):259-265.
22. Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 2007, 318(5849):467-470. 10.1126/science.1145432, 17947585.
23. Sugama N, Park JG, Park YJ, Takeuchi Y, Kim SJ, Takemura A. Moonlight affects nocturnal Period2 transcript levels in the pineal gland of the reef fish Siganus guttatus. Journal of Pineal Research 2008, 45(2):133-141. 10.1111/j.1600-079X.2008.00566.x, 18298465.
24. Neumann D. Physiologische Uhren von Insekten - Zur Ökophysiologie lunarperiodisch kontrollierter Fortpflanzungszeiten. Naturwissenschaften 1995, 82(7):310-320.
25. Neumann D, Heimbach F. Time Cues for Semilunar Reproduction Rhythms in European Populations of Clunio marinus. I. The Influence of Tidal Cycles of Mechanical Disturbance. Cyclic Phenomena in Marine Plants and Animals 1979, 423-433. Oxford and New York: Pergamon Press, Naylor E, Hartnoll RG.
26. Neumann D, Heimbach F. Time Cues for Semilunar Reproduction Rhythms in European Populations of Clunio marinus 2. The Influence of Tidal Temperature Cycles. Biological Bulletin 1984, 166(3):509-524.
27. Neumann D. Genetic adaptation in emergence time of Clunio populations to different tidal conditions. Helgoländer wissenschaftliche Meeresuntersuchungen 1967, 15(1-4):163-171.
28. Neumann D. Photoperiodic influences of the moon on behavioural and developmental performances of organisms. Internetional Journal of Biometeorology 1985, 29(Suppl 2):165-177.
29. Emerson KJ, Bradshaw WE, Holzapfel CM. Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. Trends in Genetics 2009, 25(5):217-225. 10.1016/j.tig.2009.03.009, 19375812.
30. Neumann D. Circadian Components of Semilunar and Lunar Timing Mechanisms. Journal of Biological Rhythms 1989, 4(2):285-294.
31. Neumann D. Phase Response Curves (PRCs) of Clunio marinus. An Atlas of Phase Responses Curves for Circadian and Circatidal Rhythms 1990, 715. Nashville: Department of Biology, Vanderbilt University, Johnson CH.
32. Pittendrigh CS. Circadian Systems. I. Driving Oscillation and Its Assay in Drosophila Pseudoobscura. Proceedings of the National Academy of Sciences of the United States of America 1967, 58(4):1762-1767. 10.1073/pnas.58.4.1762, 223992, 5237901.
33. Neumann D. Combination of Different Endogenous Rhythms in Temporal Programming of Development and Behaviour. Oecologia 1969, 3(2):166-183.
34. Neumann D. Physiological Clocks of Insects - Ecophysiology of Reproductive Activities Controlled by Lunar Cycles. Naturwissenschaften 1995, 82(7):310-320.
35. Bünning E. Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Berichte der Deutschen Botanischen Gesellschaft 1936, 54:590-596.
36. Tauber E, Kyriacou BP. Insect photoperiodism and circadian clocks: Models and mechanisms. Journal of Biological Rhythms 2001, 16(4):381-390. 10.1177/074873001129002088, 11506382.
37. Emerson KJ, Dake SJ, Bradshaw WE, Holzapfel CM. Evolution of photoperiodic time measurement is independent of the circadian clock in the pitcher-plant mosquito, Wyeomyia smithii. Journal of Comparative Physiology A -Neuroethology, Sensory, Neural and Behavioral Physiology 2009, 195(4):385-391.
38. Tauber E, Zordan M, Sandrelli F, Pegoraro M, Osterwalder N, Breda C, Daga A, Selmin A, Monger K, Benna C, Rosato E, Kyriacou CP, Costa R. Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 2007, 316(5833):1895-1898. 10.1126/science.1138412, 17600215.
39. Sandrelli F, Tauber E, Pegoraro M, Mazzotta G, Cisotto P, Landskron J, Stanewsky R, Piccin A, Rosato E, Zordan M, Costa R, Kyriacou CP. A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 2007, 316(5833):1898-1900. 10.1126/science.1138426, 17600216.
40. Lin JM, Kilman VL, Keegan K, Paddock B, Emery-Le M, Rosbash M, Allada R. A role for casein kinase 2 alpha in the Drosophila circadian clock. Nature 2002, 420(6917):816-820. 10.1038/nature01235, 12447397.
41. Martinek S, Inonog S, Manoukian AS, Young MW. A role for the segment polarity gene shaggy/GSK-3 in the Drosophila circadian clock. Cell 2001, 105(6):769-779. 10.1016/S0092-8674(01)00383-X, 11440719.
42. Ghavidel A, Schultz MC. TATA binding protein-associated CK2 transduces DNA damage, signals to the RNA polymerase III transcriptional machinery. Cell 2001, 106(5):575-584. 10.1016/S0092-8674(01)00473-1, 11551505.
43. Gogel S, Wakefield S, Tear G, Klambt C, Gordon-Weeks PR. The Drosophila microtubule associated protein Futsch is phosphorylated by Shaggy/Zeste-white 3 at an homologous GSK3 beta phosphorylation site in MAP1B. Molecular and Cellular Neuroscience 2006, 33(2):188-199. 10.1016/j.mcn.2006.07.004, 16949836.
44. Willert K, Brink M, Wodarz A, Varmus H, Nusse R. Casein kinase 2 associates with and phosphorylates dishevelled. EMBO Journal 1997, 16(11):3089-3096. 10.1093/emboj/16.11.3089, 1169927, 9214626.
45. Siegfried E, Chou TB, Perrimon N. Wingless Signaling Acts through Zeste-White 3, the Drosophila Homolog of Glycogen-Synthase Kinase-3, to Regulate Engrailed and Establish Cell Fate. Cell 1992, 71(7):1167-1179. 10.1016/S0092-8674(05)80065-0, 1335365.
46. Michailova P. Comparative External Morphological and Karyological Characteristics of European Species of Genus Clunio HALIDAY 1855. VII International Symposium of Chironomidae 1980, 9-15.
47. Zuther P, Gorbey S, Lemmer B. Chronos-Fit 1.06. 2009, http://www.chronopharmacology.de/software.htm
48. Krüger M, Neumann D. The temperature-dependence of semilunar and diurnal eclosion rhythms in the intertidal midge Clunio marinus (Diptera, Chironomidae). Helgoländer Meeresuntersuchungen 1983, 36(4):427-464.
49. Pittendrigh CS. Circadian Systems: Entrainment. Handbook of Behavioural Neurobiology 1981, 57-80. New York: Plenum Press, Aschoff J.
50. Saunders DS. Insect clocks. 2002, Amsterdam: Elsevier.
51. Neumann D. Temperature compensation of circasemilunar timing in the intertidal insect Clunio. Journal of Comparative Physiology A - Sensory Neural and Behavioral Physiology 1988, 163(5):671-676.
52. Crawley MJ. The R Book. 2007, Chichester: John Wiley & Sons Ltd.
53. Heimbach F. Semilunare und diurnale Schlüpfrhythmen südenglischer und norwegischer Clunio-Populationen (Diptera, Chironomidae). PhD thesis 1976, Köln: Universität Köln.