Tracking the seasons: the internal calendars of vertebrates

Abstract

Animals have evolved many season-specific behavioural and physiological adaptations that allow them to both cope with and exploit the cyclic annual environment. Two classes of endogenous annual timekeeping mechanisms enable animals to track, anticipate and prepare for the seasons: a timer that measures an interval of several months and a clock that oscillates with a period of approximately a year. Here, we discuss the basic properties and biological substrates of these timekeeping mechanisms, as well as their reliance on, and encoding of environmental cues to accurately time seasonal events. While the separate classification of interval timers and circannual clocks has elucidated important differences in their underlying properties, comparative physiological investigations, especially those regarding seasonal prolactin secretions, hint at the possibility of common substrates.

Figure 1

Annual timekeeping mechanisms. (a) Interval timer of the Siberian hamster. (1) Decreasing day lengths trigger the interval timer/induce the winter phenotype. (2) The timer runs to completion. (3) Refractoriness/spontaneous reversion to the spring phenotype. (4) Prolonged exposure to long day lengths breaks refractoriness/resets the interval timer. (b) Circannual clock of the golden-mantled ground squirrel. Successive oscillations between the summer and winter phenotypes are driven by an endogenous clock rather than exogenous factors.

Figure 2

(a) Body mass records of two Siberian hamsters, one maintained continuously in a long day length (LD; 14 h light per day) and the other transferred to a short day length (SD; 10 h light per day) as indicated by arrow. SDs initially induce a marked decrease in body mass, but after 24 weeks body mass spontaneously reverts to LD values, even though there has been no change in environmental conditions. At this point, the hamster is unresponsive to SDs and is considered photorefractory. In contrast, maintenance in a LD results in uninterrupted body mass increases (M. J. Paul 2006, unpublished data). (b) Circannual body mass rhythm of an individual golden-mantled ground squirrel housed in a fixed photoperiod of 14 h light per day, then 12 h light per day, then constant light for the last 11 months. At year 3, the ambient temperature was changed from 23 to 6.5°C. The rhythm in body mass persists under all housing conditions (modified from Ruby et al. 1998).