Abstract
Light is essential for the survival of almost all organisms. Development of biological light detectors, called photoreceptors, allowed bacteria, plants, and animals to sense light. The evolution of the photoreceptor organs led to the appearance of visual systems. Through light perception, organisms started to adapt their behavioral and physiological processes to variations of light intensity and spectrum. Animals developed stereotypical behavioral responses to light. Profound understanding of photoreception in fruit fly Drosophila melanogaster allow to study how the light information is processed and responses are generated. In this study, we report previously undescribed color-specific behavioral responses of fruit flies to light and identify the phototransduction pathways, which are required for these responses. Coupling between daily varying external light and an endogenous time-keeping mechanism known as the circadian clock produces a periodic pattern in the locomotion activity of Drosophila. This pattern is commonly characterized by the so-called morning and evening peaks of activity. Here we show that activity patterns are punctuated by even stronger bouts of activity that are reminiscent of bursts. The bursts are more than ten standard deviations larger than basal activity and appear in two bands, on average around 2 hours after the morning peak and 2 hours before the evening peak. The bursts are virtually undetectable in population-averaged data due to the variability of their timing and short duration. We further show that the bursts are likely generated as a light response and independently of the circadian clock. Visual and nonvisual responses to light are often color specific due to the natural spectral sensitivity of photoreceptors. Adult Drosophila senses light mostly through the eyes, the ocelli, Hofbauer-Buchner eyelets and structural changes in the protein cryptochrome. These photoreceptors each have distinct activation spectra. To identify if the color of the light affects activity peaks and bursts, we measured fly locomotion patterns under different wavelengths of light. Data on the activity of flies illuminated with blue light showed an unequal effect of that light on activity peaks. Elevated movement speed of flies in blue color suggests blue light to be the possible driver of the activity bursts. In contrast, flies in green light reduced their activity. Distinct and non-uniform effects of light colors on fly activity hinted at a possible variation of Drosophila color preference with time. Typically, color preference in Drosophila is studied using phototaxis paradigms, which do not consider time dependence of the behavior. Here we show that when given a choice between blue, green and dim light, fruit flies exhibit an unexpectedly complex pattern of color preference that changes with the time of day. Flies display a strong green color preference in the morning and late afternoon, reduced green preference at midday, and a robust avoidance of blue throughout the day. We further show that the color preference depends on multiple photoreceptor systems. The peaks in green preference require visual photoreceptors. The midday reduction in green preference depends on the Transient Receptor Potential (TRP) channels dTRPA1 and Pyrexia (PYX) and is timed by the circadian clock. In contrast, blue avoidance is primarily mediated by class IV multidendritic neurons that tile the fly body. The avoidance requires the TRP channel Painless and is independent of the clock. Together, our results reveal the complexity of the Drosophila color-specific light responses and identify multiple photoreception and transduction pathways, which mediate those responses.