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. 2023 Sep 13;290(2006):20230149.
doi: 10.1098/rspb.2023.0149. Epub 2023 Sep 13.

Parametric effects of light acting via multiple photoreceptors contribute to circadian entrainment in Drosophila melanogaster

Lakshman Abhilash  1 , Orie Thomas Shafer  1
Affiliations

Parametric effects of light acting via multiple photoreceptors contribute to circadian entrainment in Drosophila melanogaster

Lakshman Abhilash et al. Proc Biol Sci. .

Abstract

Circadian rhythms in physiology and behaviour have near 24 h periodicities that must adjust to the exact 24 h geophysical cycles on earth to ensure adaptive daily timing. Such adjustment is called entrainment. One major mode of entrainment is via the continuous modulation of circadian period by the prolonged presence of light. Although Drosophila melanogaster is a prominent insect model of chronobiology, there is little evidence for such continuous effects of light in the species. In this study, we demonstrate that prolonged light exposure at specific times of the day shapes the daily timing of activity in flies. We also establish that continuous UV- and blue-blocked light lengthens the circadian period of Drosophila and provide evidence that this is produced by the combined action of multiple photoreceptors which, includes the cell-autonomous photoreceptor cryptochrome. Finally, we introduce ramped light cycles as an entrainment paradigm that produces light entrainment that lacks the large light-driven startle responses typically displayed by flies and requires multiple days for entrainment to shifted cycles. These features are reminiscent of entrainment in mammalian models systems and make possible new experimental approaches to understanding the mechanisms underlying entrainment in the fly.

Keywords: Aschoff's rule; Drosophila; circadian; constant light; parametric entrainment; skeleton photoperiods.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Entrainment to white light skeleton photoperiods. (a) Mean (±s.e.m.) locomotor activity profiles of CS (top), w1118 (middle) and yw (bottom) flies under symmetric skeleton photoperiods (left) and two asymmetric skeleton photoperiods (middle and right). The photoperiodic regimes are shown on top of the profile plots. Black shaded regions indicate darkness and white regions indicate light phases (400–500 lux) of the 24 h cycle. Note that the profiles under LD12 : 12 are replotted across panels to facilitate pair-wise comparisons. (b) Phases of the evening peak of activity for the three strains across the different photoperiodic conditions are shown. Boxplots that share the same letter are not statistically significantly different from each other. Statistical comparison of phases across all four photoperiodic conditions were done using Kruskal–Wallis tests. CS: χ32=95.05, p = 0; w1118: χ32=123.47, p = 0; yw: χ32=113.58, p = 0. Profiles and phases of evening peak of activity are pooled from two independent replicate runs for each genotype.
Figure 2.
Figure 2.
Free-running locomotor activity rhythms of flies under constant UV- and blue-blocked light. (a) Dose-dependent effect of constant light on the free-running period of CS (left), w1118 (middle) and yw (right) flies. The lack of data point for highest intensity of light in yw flies is because flies were arrhythmic under this condition. The yellow dashed line is dose response curve fitted through a logistic model (see Methods). ANOVAs on the fitted logistic model revealed a statistically significant effect of intensity on the free-running period for all three genotypes (CS: p < 2 × 10−16; w1118: p < 2 × 10−16; yw: p < 2 × 10−16). (b) Representative actograms of Canton-S (CS), w1118, yw, yw;;cryOUT, w;;glass[60j] and + ;;norpA[7] flies under constant darkness (top) and constant UV- and blue-blocked light (bottom) of 30-45 µW cm−2. (c) Frequency distributions of free-running periods of all genotypes under constant dark and constant light conditions. The dots and dashed vertical lines represent the median values of free-running periods under each regime. Statistical comparisons are based on Wilcoxon's tests (CS: W = 2676.5, p = 6.036 × 10−08; w1118: W = 502, p = 2.2 × 10−16; yw: W = 618.5, p = 1.583 × 10−08; yw;;cryOUT: W = 7391, p = 2.233 × 10−08; w;;glass[60j]: W = 305, p = 1.092 × 10−05; + ;;norpA[7]: W = 10, p = 2.2 × 10−16). Values are pooled from at least two independent runs (see electronic supplementary material, table S1).
Figure 3.
Figure 3.
Entrainment to ramped UV- and blue-blocked light cycles. (a) Mean (±s.e.m.) locomotor activity profiles of entrained CS (left), w1118 (middle) and yw (right) flies under ramped light cycles (top) and on the first day under constant low intensity light (bottom). (b) Polar plots showing the phases of the predominant peak of locomotor activity for the three genotypes (CS, left; w1118, middle; yw, right) under entrainment and on the first day post entrainment under constant conditions. Phase control was statistically examined using V-tests (see Methods). CS: p = 7.67 × 10−17; w1118: p = 1.45 × 10−10; yw: p = 7.38 × 10−10. (c) Representative actograms showing rhythmic and arrhythmic flies under ramped cycles for loss-of-function clock mutants. The red dashed line indicates the offset of locomotor activity. The shading on the actograms represents the ramping up and down of light, starting at Zeitgeber Time (ZT) 00. (d) Mean (±s.e.m.) locomotor activity profile (left) and polar plot depicting phases of the peak of activity of per01 flies under ramped light cycles. The black dashed line in the top row of (a) and (d-left) is a schematic of light ramping from a lower minimum value (approx. 10 µW cm−2) at ZT00 to the maximum value (40–50 μW cm−2) at ZT12 and back to the minimum value by ZT24. In all the polar plots, individual dots represent a single fly and the line from the centre points to the mean phase across all flies. The distance of these lines from the centre is an estimate of the across-fly variation in phase. Values close to 1 (grey dashed circle) have lower variances.
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