Circadian window of opportunity: what have we learned from insects?

Diurnal rhythms in plants and animals have been observed for centuries, but their endogenous and circadian nature were not acknowledged until the 1960s (Menaker, 1969). Research during that decade provided ample evidence for an internal ‘clock’ generating daily rhythms in behavior through biochemistry; however, the nature and anatomical location of this clock were a mystery. Insects helped to unveil this paradox, providing critical early insights into both the genetic and the physiological bases of the clock. The discovery of the first circadian clock gene period in Drosophila melanogaster was a milestone for chronogenetics (Konopka and Benzer, 1971). The overt behavior used to identify arrhythmic period mutants in flies was the rhythm of emergence of the adult from its pupal cuticle. This event, termed eclosion, is ‘gated’ by the circadian clock, which means that it can only occur in a restricted portion of a day/night cycle. This daily window of time is species specific; for example, D. melanogaster adults eclose in the early morning. Then, as now, D. melanogaster was an excellent organism to probe the genetic nature of the clock, but too tiny to explore the clock’s physiological and anatomical nature with the resources available at the time. This quandary was approached by young James Truman working at Harvard with Lynn Riddiford. Using two species of silk moths which eclose at different times of day, they showed that eclosion gating is governed by the brain. By exchanging brains between the two species they ‘transplanted’ the timing of eclosion. These experiments provided compelling evidence that the moth brain contains a photoreceptor mechanism, a clock and a neuroendocrine output that are necessary and sufficient for the synchronization of eclosion behavior with the environmental photoperiod (Truman and Riddiford, 1970).