Evolution of photoperiodic time measurement is independent of the circadian clock in the pitcher-plant mosquito, Wyeomyia smithii
- 134 Downloads
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.
KeywordsGeographic variation Biological clocks Seasonality Diapause Photoperiodism
Response to Nanda–Hamner protocols
Number of hours of light (L) and dark (D) in a given environmental cycle
Total numbers of hours in a given environmental cycle (T = L + D)
Akiake’s Information Criterion
Log-likelihood of a given model
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
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
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.
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.
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.
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).
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.
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).
Total period of light plus dark = L + D of an L:D = light:dark cycle.
- Anonymous (1960) Biological clocks. The Biological Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
- Bünning E (1936) Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590–607Google Scholar
- Bünning E (1964) The physiological clock. Springer, BerlinGoogle Scholar
- 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
- Danks HV (1987) Insect dormancy: an ecological perspective. Biological Survey of Canada (terrestrial arthropods), OttawaGoogle Scholar
- Edmunds LN (1988) Cellular and molecular bases of biological clocks: models and mechanisms for circadian timekeeping. Springer, New YorkGoogle Scholar
- 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
- Lane J (1953) Neotropical Culicidae. University of São Paulo, São PauloGoogle Scholar
- Menaker M (1971) Biochronometry. National Academy of Sciences, Washington, DCGoogle Scholar
- 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
- R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Roff DA (1992) The evolution of life-histories: theory and analysis. Chapman and Hall, New YorkGoogle Scholar
- Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
- Rose MR (1991) Evolutionary biology of aging. Chapman & Hall, New YorkGoogle Scholar
- Saunders DS (2002) Insect clocks. Elsevier Science, AmsterdamGoogle Scholar
- 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
- Withrow RB (1959) Photoperiodism and related phenomena in plants and animals. American Association for the Advancement of Science, Washington, DCGoogle Scholar