The photoperiodic responses of Drosophila auraria are shown to involve its circadian system functioning as the “clock” that measures the duration of darkness at night. Attempts at further clarification of this finding were based on the widely held assumption that adaptive adjustment of critical night length is caused by change in the circadian system's entrainment behavior. Three different experimental programs yielded data that are incompatible with this starting premise. Collectively, the observations suggest a new interpretation of the lability (phenotypic and genetic) of critical night length based on change in the level of response to all night-length measurements—not on the measurements themselves. This proposition is found especially relevant to the temperature dependence of photoperiodic responses and its role in controlling the onset and termination of the breeding season at different latitudes.