A brief history of circannual time.

Innate circannual timing is an ancestral trait that first evolved in free-living eukaryotic cells some 2000 million years ago, with marine algae of the genus Allexandrium providing a living unicellular model. This species shows the primitive trait of 'alternation of generations', where the organism alternates between fast replicating vegetative cells in the summer and a dormant cystic cell over the winter. The resistant cysts sink into the cold ocean sediments. Remarkably, excystment in spring is governed by an endogenous circannual timing mechanism. Thus, a tiny, short-lived unicell can utilise a circannual clock as part of the life-history programme of the species. Innate timing allows for major adjustments in physiology and behaviour in anticipation of the seasons, and provides an internalised sense of seasonal time for the many species where standard environmental cues are weak or ambiguous. This is a highly adaptive strategy irrespective of the size and longevity of an organism. Circannual rhythms are expressed by a diverse range of organisms, from flowering plants to mammals, interwoven into the life-history programme of each species, being a consequence of forever living in a periodic world. In complex vertebrates, the early division of the zygote potentially carries circannual timer genes into all progeny cells and tissues. This supports the concept of a 'clock-shop' where cell-autonomous long-term rhythms are generated in each tissue, orchestrated by a central circannual pacemaker system. This is analogous to the organisation of the circadian timing system. For the circannual time-scale, specialised thyrotroph cells located in the pars tuberalis of the pituitary gland and adjacent tanycyte cells located in the ependymal wall of the third cerebral ventricle of the brain act as putative central circannual pacemakers. At a molecular level, epigenetically regulated, cyclical remodelling of chromatin, which determines whether specific circannual timer genes are transcriptionally active, or not, is considered to drive the oscillation between the summer and winter phenotypes.