Eur. J. Entomol. 118: 1-13, 2021 | DOI: 10.14411/eje.2021.001

Insect photoperiodism: Bünning's hypothesis, the history and development of an ideaReview

David SAUNDERS
21, Leadervale Road, Edinburgh EH16 6PB, Scotland, United Kingdom; e-mail: david59.saunders@mypostoffice.co.uk

In insects, the photoperiodic system comprises a linked sequence of events from photoreception to final seasonally-appropriate phenotypes such as overwintering diapause. The first and last of these events are reasonably well known, but central phenomena such as those distinguishing short from long days (time measurement) and the nature, accumulation and transfer of this information through development, metamorphosis and sometimes across generations remains obscure. Bünning's intuitive suggestion that photoperiodic time measurement was a function of the circadian system, made eight decades ago, however, has provided a framework for numerous studies investigating these connections. This review examines the development of Bünning's hypothesis from its origin in plants to the physiology of diapause in insects. Despite considerable inter-species differences, a close and probably causal relationship between circadian rhythmicity and photoperiodism is indicated.

Keywords: Insects, photoperiodism, diapause, Bünning's hypothesis, clock models

Received: November 30, 2020; Revised: January 6, 2021; Accepted: January 6, 2021; Published online: January 21, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SAUNDERS, D. (2021). Insect photoperiodism: Bünning's hypothesis, the history and development of an idea. EJE, 118, Article 1-13. https://doi.org/10.14411/eje.2021.001
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Adkisson P.L. 1964: Action of the photoperiod in controlling insect diapause. - Am. Nat. 98: 357-374. Go to original source...
    2. Adkisson P.L. 1966: Internal clocks and insect diapause. - Science 154: 234-241. Go to original source...
    3. Baker J.R. & Ranson R.M. 1932: Factors affecting the breeding of the field mouse (Microtus agrestis). Part 1. - Proc. R. Soc. Lond. 110: 313-323. Go to original source...
    4. Beck S.D. 1962: Photoperiodic induction of diapause in an insect. - Biol. Bull. 122: 1-12. Go to original source...
    5. Blaney L.T. & Hamner K.C. 1957: Inter-relations among the effects of temperature, photoperiod, and dark period on floral initiation of Biloxi soybean. - Bot. Gaz. 119: 10-24. Go to original source...
    6. Bowen M.F., Saunders D.S., Bollenbacher W.E. & Gilbert L.I. 1984: In vitro reprogramming of the photoperiodic clock in an insect brain-retrocerebral complex. - Proc. Natn. Acad. Sci. USA 81: 5881-5884. Go to original source...
    7. Bünning E. 1936: Die endogene Tagesrhythmik als Grundlage der Photoperiodischen Reaktion. - Ber. Dt. Bot. Ges. 54: 590-607. Go to original source...
    8. Bünning E. 1960: Circadian rhythms and time measurement in photoperiodism. - Cold Spring Harb. Symp. Quant. Biol. 25: 249-256. Go to original source...
    9. Bünning E. 1969: Common features of photoperiodism in plants and animals. - Photochem. Photobiol. 9: 219-228. Go to original source...
    10. Bünsow R.C. 1953: Uber Tages- und Jahresrhythmische Anderungen der Photoperiodischen Lichteropfindlichkeit bei Kalanchoë blossfeldiana und ihre Beziehungen zur endogenen Tagesrhythmik. - Z. Bot. 41: 257-276.
    11. Chandrashekaran M.K. 2006: Erwin Bünning (1906-1990): A centennial homage. - J. Biosci. 31: 5-12. Go to original source...
    12. Claes H. & Lang A. 1947: Die Blütenbildung von Hyoscyamus niger in 48-stündigen Licht-Dunkel-Zyklen und in Zyklen mit aufgeteilten Lichtphasen. - Z. Naturforsch. (B) 2: 56-68. Go to original source...
    13. Danilevskii A.S., Goryshin N.I. & Tyshchenko V.P. 1970: Biological rhythms in terrestrial arthropods. - Annu. Rev. Entomol. 15: 201-244. Go to original source...
    14. Darwin C. & Darwin F. 1880: The Power of Movement in Plants. John Murray, London, 593 pp. Go to original source...
    15. De Mairan J.J. 1729: Observations botaniques. - Hist. Acad. Roy. Soc. 1729: 35-36.
    16. Garner W.W. & Allard H.A. 1920: Effects of the relative length of the day and night and other factors of the environment on growth and reproduction in plants. - J. Agric. Res. 18: 553-606. Go to original source...
    17. Gibbs D. 1975: Reversal of pupal diapause in Sarcophaga argyrostoma by temperature shifts after puparium formation. - J. Insect Physiol. 21: 1179-1186. Go to original source...
    18. Goto S.G. 2013: Roles of circadian clock genes in insect photoperiodism. - Entomol. Sci. 16: 1-16. Go to original source...
    19. Goto S.G. & Numata H. 2009: Possible involvement of distinct photoreceptors in the photoperiodic induction of diapause in the flesh fly Sarcophaga similis. - J. Insect Physiol. 55: 401-407. Go to original source...
    20. Hall J.C. 2003: Genetics and molecular biology of rhythms in Drosophila and other insects. - Adv. Genet. 48: 1-280. Go to original source...
    21. Hamner K.C. 1960: Photoperiodism and circadian rhythms. - Cold Spring Harb. Symp. Quant. Biol. 25: 269-277. Go to original source...
    22. Hamner W.M. 1963: Diurnal rhythms and photoperiodism in testicular recrudescence of the house finch. - Science 142: 1294-1295. Go to original source...
    23. Hardin P.E. 2005: The circadian timekeeping system of Drosophila. - Curr. Biol. 15: R714-722. Go to original source...
    24. Kauranan H., Kinnunen J., Hillos A.-L., Lankinen P., Hopkins D., Wiberg R.A.W., Ritchie M.G. & Hoikkala A. 2019: Selection for reproduction under short photoperiods changes diapause-associated traits and induces widespread genomic divergence. - J. Exp. Biol. 222: 205831, 14 pp. Go to original source...
    25. Kogure M. 1933: The influence of light and temperature on certain characters of the silk-worm, Bombyx mori. - J. Dept. Agr. Kyushu Univ. 4: 1-93. Go to original source...
    26. Konopka R. & Benzer S. 1971: Clock mutants of Drosophila melanogaster. - Proc. Natn. Acad. Sci. USA 68: 2112-2116. Go to original source...
    27. Lees A.D. 1965: Is there a circadian component in the Megoura photoperiodic clock? In Aschoff J. (ed.): Circadian Clocks. North-Holland, Amsterdam, pp. 351-356.
    28. Lees A.D. 1966: The control of polymorphism in aphids. - Adv. Insect Physiol. 3: 207-277. Go to original source...
    29. Lees A.D. 1971: The relevance of action spectra in the study of insect photoperiodism. In Menaker M. (ed.): Biochronometry. National Academy of Sciences, Washington, pp. 372-380.
    30. Lees A.D. 1973: Photoperiodic time measurement in the aphid Megoura viciae. - J. Insect Physiol. 19: 2279-2316. Go to original source...
    31. Lees A.D. 1986: Some effects of temperature on the hour glass photoperiod timer in the aphid Megoura viciae. - J. Insect Physiol. 32: 79-89. Go to original source...
    32. Lewis R.D. & Saunders D.S. 1987: A damped circadian oscillator model of an insect photoperiodic clock. I. Description of the model based on a feedback control system. - J. Theor. Biol. 128: 47-59. Go to original source...
    33. Marcovitch S. 1923: Plant lice and light exposure. - Science 58: 537-538. Go to original source...
    34. Marcovitch S. 1924: The migration of the Aphididae and the appearance of sexual forms as affected by the relative length of daily light exposure. - J. Agric. Res. 27: 513-522.
    35. Melchers G. 1956: Die Beteiligung der endonomen Tagesrhythmik am Zustandekommen der photoperiodischen Reaktion der Kurztagpflanze Kalanchoë blossfeldiana. - Z. Naturforsch. (B) 11: 544-548. Go to original source...
    36. Nanda K.K. & Hamner K.C. 1958: Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soybean. - Bot. Gaz. 120: 14-25. Go to original source...
    37. Numata H. & Hidaka T. 1983: Compound eyes as the photoperiodic receptors in the bean bug. - Experientia 39: 868-869. Go to original source...
    38. Peterson E.L. & Saunders D.S. 1980: The circadian eclosion rhythm in Sarcophaga argyrostoma: a limit cycle representation of the pacemaker. - J. Theor. Biol. 86: 265-277. Go to original source...
    39. Pittendrigh C.S. 1965: On the mechanism of entrainment of a circadian rhythm by light cycles. In Aschoff J. (ed.): Circadian Clocks. North-Holland, Amsterdam, pp. 277-297.
    40. Pittendrigh C.S. 1966: The circadian oscillation in Drosophila pseudoobscura pupae: a model for the photoperiodic clock. - Z. Pflanzenphysiol. 54: 275-307.
    41. Pittendrigh C.S. 1972: Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. - Proc. Natn. Acad. Sci. USA 69: 2734-2737. Go to original source...
    42. Pittendrigh C.S. 1981: Circadian organization and the photoperiodic phenomena. In Follett B.K. & Follett D.E. (eds): Biological Clocks in Seasonal Reproductive Cycles. John Wright & Sons, Bristol, pp. 1-35.
    43. Richard D.S. & Saunders D.S. 1987: Prothoracic gland function in diapause and nondiapause Sarcophaga argyrostoma and Calliphora vicina. - J. Insect Physiol. 33: 385-392. Go to original source...
    44. Richard D.S., Warren J.T., Saunders D.S. & Gilbert L.I. 1987: Haemolymph ecdysteroid titres in diapause and nondiapause destined larvae and pupae of Sarcophaga argyrostoma. - J. Insect Physiol. 33: 115-122. Go to original source...
    45. Rowan W. 1926: On photoperiodism, reproductive periodicity and the annual migration of birds and certain fishes. - Proc. Soc. Nat. Hist. 38: 147-189.
    46. Saunders D.S. 1965: Larval diapause of maternal origin: Induction of diapause in Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). - J. Exp. Biol. 42: 495-508. Go to original source...
    47. Saunders D.S. 1966: Larval diapause of maternal origin - II. The effect of photoperiod and temperature on Nasonia vitripennis. - J. Insect Physiol. 12: 569-581. Go to original source...
    48. Saunders D.S. 1968: Photoperiodism and time measurement in the parasitic wasp, Nasonia vitripennis. - J. Insect Physiol. 14: 433-450. Go to original source...
    49. Saunders D.S. 1970: Circadian clock in insect photoperiodism. - Science 169: 601-603. Go to original source...
    50. Saunders D.S. 1971: The temperature compensated photoperiodic clock 'programming' development and pupal diapause in the flesh-fly, Sarcophaga argyrostoma. - J. Insect Physiol. 17: 801-812. Go to original source...
    51. Saunders D.S. 1973a: The photoperiodic clock in the flesh fly Sarcophaga argyrostoma. - J. Insect Physiol. 19: 1941-1954. Go to original source...
    52. Saunders D.S. 1973b: Thermoperiodic control of diapause in an insect: theory of internal coincidence. - Science 181: 358-360. Go to original source...
    53. Saunders D.S. 1974: Evidence for 'dawn' and 'dusk' oscillators in the Nasonia photoperiodic clock. - J. Insect Physiol. 20: 77-88. Go to original source...
    54. Saunders D.S. 1975: Spectral sensitivity and intensity thresholds in Nasonia photoperiodic clock. - Nature 233: 732-734. Go to original source...
    55. Saunders D.S. 1978a: An experimental and theoretical analysis of photoperiodic induction in the flesh-fly, Sarcophaga argyrostoma. - J. Comp. Physiol (A) 124: 75-95. Go to original source...
    56. Saunders D.S. 1978b: Internal and external coincidence and the apparent diversity of photoperiodic clocks in insects. - J. Comp. Physiol. (A) 127: 197-207. Go to original source...
    57. Saunders D.S. 1979a: The circadian eclosion rhythm in Sarcophaga argyrostoma: delineation of the responsive period for entrainment. - Physiol. Entomol. 4: 263-274. Go to original source...
    58. Saunders D.S. 1979b: External coincidence and the photoinducible phase in the Sarcophaga photoperiodic clock. - J. Comp. Physiol. (A) 132: 179-189. Go to original source...
    59. Saunders D.S. 1981: Insect photoperiodism: the clock and the counter. - Physiol. Entomol. 6: 99-116. Go to original source...
    60. Saunders D.S. 1982a: The effect of ultra-short photoperiods on the seasonal clock in Sarcophaga argyrostoma. - J. Comp. Physiol. (A) 145: 421-429. Go to original source...
    61. Saunders D.S. 1982b: Photoperiodic induction of pupal diapause in Sarcophaga argyrostoma: temperature effects on circadian resonance. - J. Insect Physiol. 28: 305-310. Go to original source...
    62. Saunders D.S. 1984: Photoperiodic time measurement in Sarcophaga argyrostoma: An attempt to use daily temperature cycles to distinguish external from internal coincidence. - J. Comp. Physiol. (A) 154: 789-794. Go to original source...
    63. Saunders D.S. 1987a: Insect photoperiodism: the linden bug, Pyrrhocoris apterus, a species that measures daylength rather than nightlength. - Experientia 43: 935-937. Go to original source...
    64. Saunders D.S. 1987b: Maternal influence on the incidence and duration of larval diapause in Calliphora vicina. - Physiol. Entomol. 12: 331-338. Go to original source...
    65. Saunders D.S. 1992: The photoperiodic clock and "counter" in Sarcophaga argyrostoma: experimental evidence consistent with "external coincidence" in insect photoperiodism. - J. Comp. Physiol. (A) 170: 121-127. Go to original source...
    66. Saunders D.S. 2002: Insect Clocks. 3rd ed. Elsevier, Amsterdam, 560 pp.
    67. Saunders D.S. 2013: Insect photoperiodism: Measuring the night. - J. Insect Physiol. 59: 1-10. Go to original source...
    68. Saunders D.S. 2016: The formal 'structure' and function of the insect photoperiodic clock: a tribute to Colin S. Pittendrigh. - Physiol. Entomol. 41: 1-18. Go to original source...
    69. Saunders D.S. 2020: Dormancy, diapause, and the role of the circadian system in insect photoperiodism. - Annu. Rev. Entomol. 65: 19.1-19.17. Go to original source...
    70. Saunders D.S. & Bertossa R.C. 2011: Deciphering time measurement: the role of circadian 'clock' genes and formal experimentation in insect photoperiodism. - J. Insect Physiol. 57: 557-566. Go to original source...
    71. Saunders D.S. & Lewis R.D. 1987a: A damped circadian oscillator model of an insect photoperiodic clock. II. Simulations of the shapes of the photoperiodic response curves. - J. Theor. Biol. 128: 61-71. Go to original source...
    72. Saunders D.S. & Lewis R.D. 1987b: A damped circadian oscillator model of an insect photoperiodic clock. III. Circadian and "hourglass" responses. - J. Theoret. Biol. 128: 73-85. Go to original source...
    73. Saunders D.S. & Lewis R.D. 1988: The photoperiodic clock and counter mechanism in two species of flies: evidence for damped circadian oscillators in time measurement. - J. Comp. Physiol. (A) 163: 365-371. Go to original source...
    74. Takimoto A. & Hamner K.C. 1964: Effect of temperature and preconditioning on photoperiodic response of Pharbitis nil. - Plant Physiol. 39: 1024-1030. Go to original source...
    75. Tyshchenko V.P. 1966: Two-oscillatory model of the physiological mechanism of insect photoperiodic reaction. - Zhur. Obshch. Biol. 27: 209-222 [in Russian].
    76. Tyukmaeva V., Lankinen P., Kinnunen J., Kauranan H. & Hoikkala A. 2020: Latitudinal clines in the timing and temperature-sensitivity of photoperiodic diapause in Drosophila montana. - Ecography 43: 1-11. Go to original source...
    77. Vaz Nunes M. & Saunders D.S. 1999: Photoperiodic time measurement in insects: a review of clock models. - J. Biol. Rhythms 14: 84-104. Go to original source...
    78. Vaze K.M. & Helfrich-Förster C. 2016: Drosophila ezoana uses an hour-glass or highly damped circadian clock for measuring night length and inducing diapause. - Physiol. Entomol. 41: 378-389. Go to original source...
    79. Werren J.H. & Loehlin D.W. 2009: The parasitoid wasp Nasonia: an emerging model species with haploid male genetics. - Cold Spring Harb. Protoc. 10: 134, 31 pp. Go to original source...
    80. Winfree A.T. 1970: Integrated view of resetting a circadian clock. - J. Theor. Biol. 28: 327-374. Go to original source...
    81. Yamaguchi K. & Goto S.G. 2019: Distinct physiological mechanisms induce latitudinal and sexual differences in the photoperiodic induction of diapause in a fly. - J. Biol. Rhythms 34: 293-306. Go to original source...
    82. Yamamoto M., Shiga S. & Goto S.G. 2017: Distribution of PERIOD-immunoreactive neurons and temporal change of the immunoreactivity under long-day and short-day conditions in the larval brain of the flesh fly Sarcophaga similis. - Chronobiol. Internat. 34: 819-825. Go to original source...
    83. Zinn J.G. 1759: Von dem Schlafe der Pflanzen. - Hamburgisches Magazin 22: 40-50.

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content