Natural Zeitgebers cannot compensate for the loss of a functional circadian clock in timing of a vital behaviour inDrosophila

Abstract

The adaptive significance of adjusting behavioural activities to the right time of the day is intuitive.Laboratory studies have implicated an important role of circadian clocks in behavioural timing and rhythmicity. Yet, recent studies on clock-mutant animals questioned this importance under more naturalistic settings, as various clock mutants showed nearly normal diel activity rhythms under semi-natural Zeitgeber conditions.We here report evidence that proper timing of eclosion, a vital behaviour of the fruit fly Drosophila melanogaster, requires a functional molecular clock even under quasi-natural conditions. In contrast to wildtype flies, period 01 mutants with a defective molecular clock eclose mostly arrhythmically in a temperate environment even in the presence of a full complement of abiotic Zeitgebers. Moreover, period 01 mutants eclose during a much larger portion of the day, and peak eclosion time becomes more susceptible to variable day-to-day changes of light and temperature. Under the same conditions, flies with impaired peptidergic inter-clock signalling (pdf 01 and han 5304 mutants) stayed largely rhythmic with normal gate sizes. Our results suggest that the presence of natural Zeitgebers can mitigate a loss of peptide-mediated phasing between central clock neuron groups, but cannot substitute for the lack of a functional molecular clock under natural temperate conditions. BackgroundEndogenous timing via circadian clocks confers adaptive advantages as it allows organisms to anticipate daily changes in the environment (see [1][2][3]). In terms of behaviour, the fitness relevance of being able to schedule locomotor activity, feeding, mating or other actions at the right time of the day is intuitive as it may help maximize success and reduce risks. Many studies under constant laboratory conditions have revealed a key role of the central and peripheral clocks in timing of behaviours across taxa. However, the importance of circadian clocks in daily timing of behaviours under natural conditions or in ecological context has come under debate, as studies in the last decade have assessed the functional importance of endogenous clocks under (semi-) natural conditions in a variety of mostly vertebrate species (see [1,2,4]). One important conclusion derived from these studies is that diel activity rhythms can remarkably differ between seminatural and laboratory conditions, since the phase relationship between behavioural activity and a given Zeitgeber such as light is modulated by other abiotic Zeitgebers, particularly by temperature [5]. Furthermore, intraand interspecific interactions such as predation [6][7][8] or competition for food [9] determine ("mask") activity patterns in the wild. Most strikingly, under semi-natural conditions in an outdoor enclosure, Per2 BRDM1 mice carrying a mutation in a core clock gene showed the same activity pattern as controls, and both showed mostly diurnal feeding, although they are strongly nocturnal in laboratory conditions [10]. In the wild, chipmunks with a lesion in t...

Model and Non-model Insects in Chronobiology

“…For these insects the daily temperature cycle is the most important Zeitgeber for emerging rhythmically from their pupal case and at least solitary bees do not entrain to LD cycles when they are present (Tweedy and Stephen, 1970;Beer et al, 2019). Even fruit flies, which can perceive light through their pupal case and which are nicely entrainable by LD cycles in the lab are very sensitive to temperature cycles (Zimmerman et al, 1968), and under natural conditions, the daily phase of eclosion and the robustness of rhythmicity depends strongly on the environmental temperature conditions (Ruf et al, 2019). This indicates that temperature cycles may be generally more important for entraining the endogenous clock of developing insects than they are for entraining the clock of adult insects.…”

Evidence for co-evolution of masking and circadian phase inDrosophila melanogaster

“…The Drosophila eclosion rhythm has been shown to be regulated by the circadian pacemakers previously implicated in activity rhythms in addition to prothoracic gland (PG) clocks (Morioka et al, 2012; Myers et al, 2003; Pittendrigh and Bruce, 1959; Selcho et al, 2017; Zimmerman et al, 1968). Additionally, in contrast to several behavioral rhythms, the act of eclosion is free from the influence of motivational state, other behaviors, or interactions among individuals, while being susceptible to disruption when mutations are introduced in core clock genes like period ( per ) or timeless ( tim ) (Qiu and Hardin, 1996; Ruf et al, 2019; Sehgal et al, 1994) both under constant and cycling conditions. Thus, relative to other rhythms, it appears to be more sensitive to perturbations in the core clock.…”

Evidence for Co-Evolution of Masking With Circadian Phase inDrosophila Melanogaster

“…The Drosophila eclosion rhythm has been shown to be regulated by the circadian pacemakers previously implicated in activity rhythms in addition to prothoracic gland clocks (Morioka et al, 2012; Myers et al, 2003; Pittendrigh and Bruce, 1959; Selcho et al, 2017; Zimmerman et al, 1968). In addition, in contrast to several behavioral rhythms, the act of eclosion is expected to be unaffected by motivational state, other behaviors, or interactions among individuals, but susceptible to disruption when mutations are introduced in core clock genes like period ( per ) or timeless ( tim ) (Qiu and Hardin, 1996; Ruf et al, 2019; Sehgal et al, 1994) both under constant and cycling conditions. Thus, relative to other rhythms, it appears to be a more reliable indicator of perturbations in the core clock.…”