Strong (Type 0) Phase Resetting of Activity-Rest Rhythm in Fruit Flies, Drosophila Melanogaster, at Low Temperature

Abstract

Amplitude modulation in limit cycle models of circadian clocks has been previously formulated to explain the phenomenon of temperature compensation. These models propose that invariance of clock period (τ) with changing temperature is a result of the system traversing small or large limit cycles such that despite a decrease or an increase in the linear velocity of the clock owing to slowing down or speeding up of the underlying biochemical reactions, respectively, the angular velocity and, thus, the clock period remain constant. In addition, these models predict that phase resetting behavior of circadian clocks described by limit cycles of different amplitudes at low or high temperatures will be drastically different. More specifically, this class of models predicts that at low temperatures, circadian clocks will respond to perturbations by eliciting larger phase shifts by virtue of their smaller amplitude and vice versa. Here, we present the results of our tests of this prediction: We examined the nature of photic phase response curves (PRCs) and phase transition curves (PTCs) for the circadian clocks of 4 wild-type fruit fly Drosophila melanogaster populations at 3 different ambient temperatures (18, 25, and 29 °C). Interestingly, we observed that at the low temperature of 18 °C, fly clocks respond to light perturbations more strongly, eliciting strong (type 0) PRCs and PTCs, while at moderate (25 °C) and high (29 °C) temperatures the same stimuli evoke weak (type 1) responses. This pattern of strong and weak phase resetting at low and high temperatures, respectively, renders support for the limit cycle amplitude modulation model for temperature compensation of circadian clocks.

Novel masking effects of light are revealed inDrosophilaby skeleton photoperiods

“…This peak is influenced by a circadian clock, but does not require it since it is observed in both wild-type and clockmutant flies. Masking effects of light can also be temperature dependent, diminishing at temperatures below 25°C (Varma et al 2013). These observations are consistent with a diurnal pattern of activity.…”

“…The circadian clock mechanism represents an adaptation to the predictable 24-h environmental cycles of light and dark, which is adjusted by various masking mechanisms in response to less predictable variation in light levels. The exogenous masking effects of light and the endogenous regulation of activity are both also temperature dependent (Vanin et al 2012;Yoshii et al 2012;Varma et al 2013) and strongly dependent on the amount of light (e.g. Bachleitner et al 2007;Kempinger et al 2009;Menagazzi et al 2012Menagazzi et al , 2013 as well as social interaction (Fujii et al 2007).…”

“…In Drosophila melanogaster, endogenous circadian clocks (Konopka & Benzer 1971;Sehgal et al 1994;Dunlap 1999;Ceriani et al 2002;Hall 2003) generate daily rhythms that can be shaped by various exogenous factors such as temperature (Vanin et al 2012;Varma et al 2013), ambient light (Bachleitner et al 2007;Reiger et al 2007;Kempinger et al 2009;Menagazzi et al 2013), and social interaction (Fujii et al 2007). Much of the research on circadian clock function has required that such exogenous factors be held constant; therefore, the mechanisms underlying their influences are not well understood.…”

Temperature–amplitude coupling for stable biological rhythms at different temperatures

“…Indeed, the magnitude of the phase shift by light was smaller at higher temperature in Neurospora [ 52 ]. Recently, the magnitude of the phase shift by light was shown to be smaller (type 1) at higher temperature than at lower temperature (type 0) in Drosophila [ 53 ]. Measurements of PRC at different temperatures can also be conducted in a circadian mammalian culture system or yeast respiration rhythms system modulated by chemical stimuli (such as forskolin or H 2 O 2 , respectively) [ 54 ].…”

Activity/rest rhythms of Drosophila populations selected for divergent eclosion timing under temperature cues

“…Therefore, one could argue that similar extent of phase variation in the stocks across different constant temperature regimes may be a consequence of similar slopes of their photic PRCs. It is known, however, that PRC amplitudes are a function of constant ambient temperatures, such that low temperatures induce large amplitude PRCs and vice versa (Lakin-Thomas et al, 1991; Varma et al, 2013). The small differences in our stocks’ response to constant temperatures could therefore indicate small differences in the way the photic PRCs change in response to temperatures.…”