Journal of Comparative Physiology A

, Volume 195, Issue 4, pp 385–391 | Cite as

Evolution of photoperiodic time measurement is independent of the circadian clock in the pitcher-plant mosquito, Wyeomyia smithii

  • Kevin J. Emerson
  • Sabrina J. Dake
  • William E. Bradshaw
  • Christina M. Holzapfel
Original Paper

Abstract

For over 70 years, researchers have debated whether the ability to use day length as a cue for the timing of seasonal events (photoperiodism) is related to the endogenous circadian clock that regulates the timing of daily events. Models of photoperiodism include two components: (1) a photoperiodic timer that measures the length of the day, and (2) a photoperiodic counter that elicits the downstream photoperiodic response after a threshold number of days has been counted. Herein, we show that there is no geographical pattern of genetic association between the expression of the circadian clock and the photoperiodic timer or counter. We conclude that the photoperiodic timer and counter have evolved independently of the circadian clock in the pitcher-plant mosquito Wyeomyia smithii and hence, the evolutionary modification of photoperiodism throughout the range of W. smithii has not been causally mediated by a corresponding evolution of the circadian clock.

Keywords

Geographic variation Biological clocks Seasonality Diapause Photoperiodism 

Abbreviations

NH

Response to Nanda–Hamner protocols

L:D

Number of hours of light (L) and dark (D) in a given environmental cycle

T

Total numbers of hours in a given environmental cycle (T = L + D)

DT

Development time

AIC

Akiake’s Information Criterion

Log(L)

Log-likelihood of a given model

Notes

Acknowledgments

We thank A. Letaw for discussion, A. Letaw and two anonymous reviewers for their comments on previous versions of this paper, and B. Kolaczkowski for valuable discussions on likelihood methods. All work presented here complied with the “Principles of animal care,” publication No. 86-23 of the National Institute of Health, and also with current laws of the United States, where these experiment were performed. This work was made possible by generous support from the National Science Foundation through grants DEB-0412573, IOB-0445710 and IOB-0520799 (REU supplement for SJD) to WEB, and the National Science Foundation and National Institutes of Health through training grants DGE-0504727 and 5-T32-GMO7413 to KJE.

Appendix: Glossary of terms highlighted in the text

Adaptive

A trait is adaptive if it is genetically determined and the possession of that trait improves fitness. We do not use adaptive or adaptation to mean phenotypically plastic, accommodative or acclimative responses of individuals to the environment

Akiake’s information criterion (AIC)

A measure of the goodness of fit of a model to a given set of data. AIC estimates the information lost by using the model rather than the data itself and, hence, lower values of AIC indicate better support of a given model.

Amplitude

One half of the difference between the maximum and minimum magnitude of a rhythm or oscillation. If the amplitude is zero, then there is no rhythm.

Critical photoperiod

The length of day that induces or maintains 50% diapause and stimulates 50% development in a sample cohort. Critical photoperiod is an overt expression of the photoperiodic timer.

Depth of diapause

Herein, the number of long-days required to terminate diapause in 50% of a sample cohort (Bradshaw and Lounibos 1977; Emerson et al. 2008b). Depth of diapause is an overt expression of the photoperiodic counter. Depth of diapause is also referred to as the intensity of diapause (Danks 1987, p. 17);

NH response

Response to Nanda–Hamner experiments in which organisms are exposed to a fixed day length and, in separate experiments with separate animals, varying night length. The phenotypic response may be either rhythmic or non-rhythmic (linear).

Period

Peak-to-peak or valley-to-valley interval of a rhythm or oscillation. If there is no significant period of oscillation, then there is no rhythm.

Pleiotropy

The influence of a locus on more than one trait. Pleiotropic effects can be assessed either by molecular genetic techniques showing the effect of a single gene on more than one phenotype, or by quantitative genetic techniques showing a correlated response to selection in the absence of linkage disequilibrium (Roff 1997).

T

Total period of light plus dark = L + D of an L:D = light:dark cycle.

References

  1. Anonymous (1960) Biological clocks. The Biological Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  2. Armbruster PA, Bradshaw WE, Holzapfel CM (1998) Effects of postglacial range expansion on allozyme and quantitative genetic variation in the pitcher-plant mosquito, Wyeomyia smithii. Evolution 52:1697–1704CrossRefGoogle Scholar
  3. Blaney LT, Hamner KC (1957) Inter-relations among the effects of temperature, photoperiod, and dark period on floral initiation of Biloxi soybean. Bot Gaz 119:10–24CrossRefGoogle Scholar
  4. Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Natl Acad Sci USA 98:14509–14511PubMedCrossRefGoogle Scholar
  5. Bradshaw WE, Holzapfel CM (2007a) Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1–25CrossRefGoogle Scholar
  6. Bradshaw WE, Holzapfel CM (2007b) Tantalizing timeless. Science 316:1851–1852PubMedCrossRefGoogle Scholar
  7. Bradshaw WE, Lounibos LP (1972) Photoperiodic control of development in the pitcher-plant mosquito, Wyeomyia smithii. Can J Zool 50:713–719CrossRefGoogle Scholar
  8. Bradshaw WE, Lounibos LP (1977) Evolution of dormancy and its photoperiodic control in pitcher-plant mosquitoes. Evolution 31:546–567CrossRefGoogle Scholar
  9. Bradshaw WE, Quebodeaux MC, Holzapfel CM (2003) Circadian rhythmicity and photoperiodism in the pitcher-plant mosquito: adaptive response to the photic environment or correlated response to the seasonal environment? Am Nat 161:735–748PubMedCrossRefGoogle Scholar
  10. Bradshaw WE, Zani PA, Holzapfel CM (2004) Adaptation to temperate climates. Evolution 58:1748–1762PubMedGoogle Scholar
  11. Bradshaw WE, Holzapfel CM, Mathias D (2006) Circadian rhythmicity and photoperiodism in the pitcher-plant mosquito: can the seasonal timer evolve independently of the circadian clock? Am Nat 167:601–605PubMedCrossRefGoogle Scholar
  12. Bünning E (1936) Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–607Google Scholar
  13. Bünning E (1964) The physiological clock. Springer, BerlinGoogle Scholar
  14. Burnham KP, Anderson DR (2004) Multimodal inference: understanding AIC and BIC in model selection. Soc Meth Res 33:261–304CrossRefGoogle Scholar
  15. Campbell MD, Bradshaw WE (1992) Genetic coordination of diapause in the pitcher-plant mosquito, Wyeomyia smithii (Diptera, Culicidae). Ann Entomol Soc Am 85:445–451Google Scholar
  16. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, Young MW (2001) Circadian regulation of gene expression systems in the Drosophila head. Neuron 32:657–671PubMedCrossRefGoogle Scholar
  17. Danks HV (1987) Insect dormancy: an ecological perspective. Biological Survey of Canada (terrestrial arthropods), OttawaGoogle Scholar
  18. Danks HV (2005) How similar are daily and seasonal biological clocks? J Insect Physiol 51:609–619PubMedCrossRefGoogle Scholar
  19. Edmunds LN (1988) Cellular and molecular bases of biological clocks: models and mechanisms for circadian timekeeping. Springer, New YorkGoogle Scholar
  20. Emerson KJ, Bradshaw WE, Holzapfel CM (2008a) Concordance of the circadian clock with the environment is necessary to maximize fitness in natural populations. Evolution 62:979–983PubMedCrossRefGoogle Scholar
  21. Emerson KJ, Letaw AD, Bradshaw WE, Holzapfel CM (2008b) Extrinsic light:dark cycles, rather than endogenous circadian cycles, affect the photoperiodic timer in the pitcher-plant mosquito, Wyeomyia smithii. J Comp Phys A 194:611–615CrossRefGoogle Scholar
  22. Hoy MA (1978) Variability in diapause attributes of insects and mites: some evolutionary and practical implications. In: Dingle H (ed) Evolution of insect migration and diapause. Springer, New York, pp 101–126Google Scholar
  23. Johnson CH, Golden SS, Ishiura M, Kondo T (1996) Circadian clocks in prokaryotes. Mol Microbiol 21:5–11PubMedCrossRefGoogle Scholar
  24. Lane J (1953) Neotropical Culicidae. University of São Paulo, São PauloGoogle Scholar
  25. Lankinen P, Forsman P (2006) Independence of genetic geographical variation between photoperiodic diapause, circadian eclosion rhythm, and Thr-Gly repeat region of the period gene in Drosophila littoralis. J Biol Rhythms 21:3–12PubMedCrossRefGoogle Scholar
  26. Mathias D, Jacky L, Bradshaw WE, Holzapfel CM (2005) Geographic and developmental variation in expression of the circadian rhythm gene, timeless, in the pitcher-plant mosquito, Wyeomyia smithii. J Insect Physiol 51:661–667PubMedCrossRefGoogle Scholar
  27. McDonald MJ, Rosbash M (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107:567–578PubMedCrossRefGoogle Scholar
  28. Menaker M (1971) Biochronometry. National Academy of Sciences, Washington, DCGoogle Scholar
  29. Nanda KK, Hamner KC (1958) Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soybean. Bot Gaz 120:14–25CrossRefGoogle Scholar
  30. Pittendrigh CS (1981) Circadian organization and the photoperiodic phenomena. In: Follett BK, Follett DE (eds) Biological clocks in seasonal reproductive cycles. Wright, Bristol, pp 1–35Google Scholar
  31. Ptitsyn AA, Zvonic S, Gimble JM (2007) Digital signal processing reveals circadian baseline oscillation in majority of mammalian genes. PLoS Comp Biol 3:e120CrossRefGoogle Scholar
  32. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  33. Roff DA (1992) The evolution of life-histories: theory and analysis. Chapman and Hall, New YorkGoogle Scholar
  34. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
  35. Rose MR (1991) Evolutionary biology of aging. Chapman & Hall, New YorkGoogle Scholar
  36. Saunders DS (1968) Photoperiodism and time measurement in the parasitic wasp, Nasonia vitripennis. J Insect Physiol 14:433–450CrossRefGoogle Scholar
  37. Saunders DS (1974) Evidence for ‘dawn’ and ‘dusk’ oscillators in the Nasonia photoperiodic clock. J Insect Physiol 20:77–88CrossRefGoogle Scholar
  38. Saunders DS (2002) Insect clocks. Elsevier Science, AmsterdamGoogle Scholar
  39. Saunders DS, Lewis RD, Warman GR (2004) Photoperiodic induction of diapause: opening the black box. Physiol Entomol 29:1–15CrossRefGoogle Scholar
  40. Sharma VK (2003) Adaptive significance of circadian clocks. Chronobiol Int 20:901–919PubMedCrossRefGoogle Scholar
  41. Stehlík J, Závodská R, Shimada K, Šauman I, Koštál V (2008) Photoperiodic induction of diapause requires regulated transcription of timeless in the larval brain of Chymomyza costata. J Biol Rhythms 23:129–139PubMedCrossRefGoogle Scholar
  42. Stone A, Knight KL, Starke H (1959) A synoptic catalog of the mosquitoes of the world (Diptera: Culicidae). Entomological Society of America, Washington, DCGoogle Scholar
  43. 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 (2007) Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316:1895–1898PubMedCrossRefGoogle Scholar
  44. Veerman A (2001) Photoperiodic time measurement in insects and mites: a critical evaluation of the oscillator-clock hypothesis. J Insect Physiol 47:1097–1109PubMedCrossRefGoogle Scholar
  45. Withrow RB (1959) Photoperiodism and related phenomena in plants and animals. American Association for the Advancement of Science, Washington, DCGoogle Scholar
  46. Yan OY, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kevin J. Emerson
    • 1
  • Sabrina J. Dake
    • 1
  • William E. Bradshaw
    • 1
  • Christina M. Holzapfel
    • 1
  1. 1.Center for Ecology and Evolutionary BiologyUniversity of OregonEugeneUSA

Personalised recommendations