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.Keywords: seasonality; photoperiodism; circannual; interval timers While the Earth remaineth, seedtime and harvest, and cold and heat, and summer and winter, and day and night shall not cease.Genesis 8: 22, King James Version (1611) As the Earth makes its yearly orbit around the Sun, the planet's 23.58 axial tilt leads to the cyclical environmental changes that we call the seasons. Recurrent challenges to the survival of organisms and their offspring arise with the dawning of each new season, and animals have evolved seasonally induced changes in phenotype that adapt them to these predictable events. For example, in many temperate environments, winter is generally characterized by severe decreases in ambient temperature and food availability, leading to increased energetic demands at a time when resources are diminished. Because energy requirements of female mammals typically increase markedly during lactation (Bronson 1989) and newly weaned offspring are particularly vulnerable to environmental perturbations (Hill 1992), raising offspring during this time of year is often futile. Thus, many temperate species have evolved winter-specific behaviours and physiology to conserve energy (e.g. hibernation, a more insulative pelage, huddling) or provide for escape (e.g. migration). Many species also increase the chances of offspring survival by timing their mating behaviours so that parturition occurs during energetically favourable times of year.

Annual rhythms that underlie phenology: biological time-keeping meets environmental change

“…This requirement for short days has been termed the breaking of refractoriness, but could also be seen as an advance of the underlying circannual system which in some species is obligatory [15,43,47]. Hence, it is not excluded that photorefractoriness, in birds and in mammals, could depend on a similar circannual timing mechanism [2,22,24].…”

“…Perhaps we have retained a circannual timer that can be synchronized by photoperiod or metabolic status [15,111,112]. Alternatively, as our ancestors moved from Africa to the higher latitudes and encountered progressively greater variation in food availability and temperature, they could have evolved a strong photoperiodic response [7,24].…”

“…Species at mid-latitude locations use photoperiod as the dominant source of temporal information. These examples were thought to fundamentally differ, but now are increasingly seen as based on common mechanisms that are modified in species-specific ways [1,[22][23][24]. Here, we present an overview of the mechanisms by which animals keep track of time to create annual phenologies, with an emphasis on birds and mammals and a focus on circannual clocks.…”

Optimal annual routines: behaviour in the context of physiology and ecology

“…There are complex interactions between the reproductive system and the environment that involve state variables other than the state of reproductive system (see Hahn & MacDougall-Shackleton 2008;Paul et al 2008;Wikelski et al 2008). Many studies of behaviour over the annual cycle have shown that cues such as short days trigger a particular phase of the life cycle (e.g.…”

Introduction. Adaptation to the annual cycle

“…In a seasonal environment, it is important for animals to control the timing of activities. Mechanisms for this are discussed by Paul et al (2008) and Wikelski et al (2008).…”