Toward a Molecular Biological Calendar?

Of all the physiological functions that involve the circadian system, none has been more extensively studied than the measurement of day length and how organisms use this photoperiodic information as a calendar to time annual processes. The stunning success in recent years of uncovering the genetic components of circadian clockworks has propelled circadian biology from the formalisms that were so important in shaping its origins to mechanisms at a molecular level. An important factor in achieving the successes to date, and one that was not necessarily to be expected, is the conservation across diverse groups not only of the features of circadian systems generally but also of their biochemical components—including gene products and gene-regulatory sequences. The clock is no longer a black box, and apart from actually understanding the clockwork itself, the next step is to link physiological functions of the clock to its molecular components. We argue below that understanding how the circadian pacemaker carries out its evident calendrical function at a molecular level is the most important problem facing those interested in photoperiodism. The irony is that the “model” species used to understand photoperiodism in plants, insects, and vertebrates are not the ones most used to analyze the molecular basis of the clockwork. Either students of photoperiodism will have to shift to more genetically amenable species (making the reasonable assumption that these organisms possess an internal calendar just as they possess an internal watch) or they will have to adapt the molecular techniques used so successfully in model systems to less genetically tractable plants and animals. This special issue on photoperiodism is structured around two interrelated themes. The early articles focus on the photoperiodic timing system of mammals, because, despite the initial preeminence of work in plants, insects, and birds, it is only in mammals that the principal anatomical and physiological elements of both circadian and photoperiodic timing are reasonably well-defined. It had often been suggested, based on formal photoperiodic analysis and neuroanatomical interventions, that the central circadian clock within the suprachiasmatic nuclei (SCN) somehow also encapsulates time of year (i.e., day length), but the exciting work described by Schwartz et al. (2001 [this issue]) now proves this beyond all reasonable doubt. As the authors readily admit, a host of questions remain to be answered at many levels. Even at the organismal level, a link between so-called endogenous circannual rhythms regulating some annual cycles in birds and mammals and photoperiodic regulation of circadian rhythms remains to be forged. What is clear, though, is that the SCN encodes day length as an integral element of the circadian waveform and this is visible in both the dynamics of cellular properties (electrophysiologically and as neurosecretion) and the dynamics of gene expression. Next come two broad problems. The first is to determine the precise molecular nature of the calendar within the SCN. The second is to determine just how the organism reads out the calendrical message and converts it into the wide range of striking physiological changes that can be observed in, for example, reproduction, food intake, or hibernation. For physiological readout, the calendrical outputs from the SCN can be either humoral or neural. Nothing is known of the humoral output in the context of calendrical information, and precious little beyond its likely existence in the context of circadian information. Only a bit more is known of the calendrical neural outputs: that they do regulate the pineal gland and cause the secretion of melatonin to reflect day length in a fairly accurate manner. Intriguingly, however,