Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 May 22;267(1447):1005–1010. doi: 10.1098/rspb.2000.1103

Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids.

F Fleury 1, R Allemand 1, F Vavre 1, P Fouillet 1, M Boulétreau 1
PMCID: PMC1690635  PMID: 10874750

Abstract

Most organisms show self-sustained circadian oscillations or biological clocks which control their daily fluctuations in behavioural and physiological activities. While extensive progress has been made in understanding the molecular mechanisms of biological clocks, there have been few clear demonstrations of the fitness value of endogenous rhythms. This study investigated the adaptive significance of circadian rhythms in a Drosophila parasitoid community. The activity rhythms of three sympatric Drosophila parasitoids are out of phase, the competitively inferior parasitoid species being active earlier than the superior competitor. This temporal segregation appears at least partially determined by endogenous periods of the clock which also vary between species and which correlate the time of activity. This earlier activity of the inferior competitor significantly reduces its intrinsic competitive disadvantage when multiparasitism occurs, thus suggesting that natural selection acting on the phase of the rhythm could substantially deviate the endogenous period from the optimal ca. 24 h period. This study demonstrates that temporal segregation of competing species could be endogenously controlled, which undoubtedly favours their coexistence in nature and also shows how natural selection can act on biological clocks to shape daily activity patterns.

Full Text

The Full Text of this article is available as a PDF (209.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allemand R., Biston J., Fouillet P. Variabilité génétique du profil circadien d'activité de la Drosophile dans une population naturelle. C R Acad Sci III. 1989;309(11):477–483. [PubMed] [Google Scholar]
  2. Czeisler C. A., Duffy J. F., Shanahan T. L., Brown E. N., Mitchell J. F., Rimmer D. W., Ronda J. M., Silva E. J., Allan J. S., Emens J. S. Stability, precision, and near-24-hour period of the human circadian pacemaker. Science. 1999 Jun 25;284(5423):2177–2181. doi: 10.1126/science.284.5423.2177. [DOI] [PubMed] [Google Scholar]
  3. Darlington T. K., Wager-Smith K., Ceriani M. F., Staknis D., Gekakis N., Steeves T. D., Weitz C. J., Takahashi J. S., Kay S. A. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science. 1998 Jun 5;280(5369):1599–1603. doi: 10.1126/science.280.5369.1599. [DOI] [PubMed] [Google Scholar]
  4. Dunlap J. C. Genetics and molecular analysis of circadian rhythms. Annu Rev Genet. 1996;30:579–601. doi: 10.1146/annurev.genet.30.1.579. [DOI] [PubMed] [Google Scholar]
  5. Dunlap J. Circadian rhythms. An end in the beginning. Science. 1998 Jun 5;280(5369):1548–1549. doi: 10.1126/science.280.5369.1548. [DOI] [PubMed] [Google Scholar]
  6. Fleury F., Allemand R., Fouillet P., Boulétreau M. Genetic variation in locomotor activity rhythm among populations of Leptopilina heterotoma (Hymenoptera: Eucoilidae), a larval parasitoid of Drosophila species. Behav Genet. 1995 Jan;25(1):81–89. doi: 10.1007/BF02197245. [DOI] [PubMed] [Google Scholar]
  7. Hall J. C. Tripping along the trail to the molecular mechanisms of biological clocks. Trends Neurosci. 1995 May;18(5):230–240. doi: 10.1016/0166-2236(95)93908-g. [DOI] [PubMed] [Google Scholar]
  8. Hamblen M. J., White N. E., Emery P. T., Kaiser K., Hall J. C. Molecular and behavioral analysis of four period mutants in Drosophila melanogaster encompassing extreme short, novel long, and unorthodox arrhythmic types. Genetics. 1998 May;149(1):165–178. doi: 10.1093/genetics/149.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hastings M. Biological rhythms. Resetting the circadian cycle. Nature. 1995 Jul 27;376(6538):296–297. doi: 10.1038/376296a0. [DOI] [PubMed] [Google Scholar]
  10. Konopka R. J., Benzer S. Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2112–2116. doi: 10.1073/pnas.68.9.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ouyang Y., Andersson C. R., Kondo T., Golden S. S., Johnson C. H. Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8660–8664. doi: 10.1073/pnas.95.15.8660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Petersen G., Hall J. C., Rosbash M. The period gene of Drosophila carries species-specific behavioral instructions. EMBO J. 1988 Dec 1;7(12):3939–3947. doi: 10.1002/j.1460-2075.1988.tb03280.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Pittendrigh C. S. Temporal organization: reflections of a Darwinian clock-watcher. Annu Rev Physiol. 1993;55:16–54. doi: 10.1146/annurev.ph.55.030193.000313. [DOI] [PubMed] [Google Scholar]
  14. Schibler U. Circadian rhythms. New cogwheels in the clockworks. Nature. 1998 Jun 18;393(6686):620–621. doi: 10.1038/31337. [DOI] [PubMed] [Google Scholar]
  15. Sokolove P. G., Bushell W. N. The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol. 1978 May 8;72(1):131–160. doi: 10.1016/0022-5193(78)90022-x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES