What season is it anyway? Circadian tracking vs. photoperiodic anticipation in insects

Abstract

The daily rhythm of 24 h and the annual rhythm of 12 mo constitute the 2 major, highly predictable rhythms of the biosphere. The internal circadian clock enables organisms to track daily changes in their environment; the photoperiodic timer, alone or in concert with a circannual clock, enables organisms to anticipate and prepare in advance for seasonal changes in their environment. The circadian clock entrains to dawn and dusk and tracks light and temperature on a day-to-day basis, while the photoperiodic timer serves as a long-term, physiological go/no-go switch that commits an animal to development, reproduction, dormancy, or migration on a seasonal or even lifetime basis. In 1936, Erwin Bünning proposed that circadian rhythms formed the basis (Grundlage) for photoperiodic response to day length. Historical inertia generated by correlative evidence from early physiological studies and a proliferating number of descriptive models has resulted in the widespread assumption that the circadian clock constitutes the necessary, causal basis of photoperiodism in general. This historical inertia has also restricted the search for genes involved in insect photoperiodism to genes central to the circadian clock in Drosophila and has led investigators to conclude that any behavior, process, or gene expression that varies with day length represents photoperiodism or a gene involved in photoperiodism. The authors discuss how blinders imposed by the circadian imperative have retarded progress toward identifying the genetic basis of photoperiodism and how the insights gained from geographic variation in photoperiodic response have been used to show the independent evolution of the circadian clock and photoperiodism. When geographic variation is found in circadian genes, the most immediate and parsimonious search for adaptive significance should be in circadian function, not in extrapolation to photoperiodism. Finally, the authors propose that circadian-unbiased, forward genetic approaches should be used to identify genes involved in photoperiodism within extant populations and among populations over evolutionary time.