The temporal 'structure' and function of the insect photoperiodic clock: a tribute to Colin S. Pittendrigh

In 1936, Erwin Bunning suggested that photoperiodic time measurement was a function of the circadian system. Colin Pittendrigh became an ardent supporter of Bunning's hypothesis, drawing parallels between photoperiodism and his own group's investigations of adult eclosion rhythmicity in the fruit fly Drosophila pseudoobscura. They developed several more modern versions of Bunning's general hypothesis based on the entrainment of circadian oscillations to the light cycle, including 'external coincidence', which is a derivation of Bunning's original model, and 'internal coincidence', which relied upon seasonal changes in the mutual phase relationship of oscillators within a multi-oscillator circadian system. This review considers the experimental evidence for the central role of the circadian system in photoperiodic timing and, in some species, for both external and internal coincidence. Pittendrigh, however, pursued the idea of internal coincidence further with his analysis of the pacemaker-slave organization of eclosion rhythmicity in D. pseudoobscura and proposed a similar theoretical model for photoperiodism comprising a group of slave oscillators driven by a light-sensitive pacemaker. In this model, the phase relationships of the slaves to the pacemaker were affected by (i) the relative periods of the pacemaker and slave(s); (ii) the strength(s) of the coupling between the two; and (iii) the dampening coefficients of the various slaves. Manipulation of these variables showed that the slaves adopted different internal phase relationships (both to each other and to the pacemaker) under the influence of changes in daily photophase, the period of the Zeitgeber and phase shifts of the entraining light cycle.