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Flies’ colour preferences depend on the time of day

Behavioural and genetic experiments have revealed that fruit flies prefer green light over other colours in the morning and evening, and always avoid blue. These colour preferences rely on different mechanisms.
Charlotte Helfrich-Förster is in the Department of Neurobiology and Genetics, Theodor Boveri Institute, Biocenter, University of Würzburg, Am Hubland, 97074 Würzburg, Germany.
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Colour vision helps animals to find nutritious food, to avoid poisonous animals and, in some cases, in social interactions1. Colour can affect people’s mood, and their colour preferences might reflect current emotional and physiological states2. Colour preferences also seem to vary through the seasons3. Writing in Nature, Lazopulo et al.4 show that the fruit fly Drosophila avoids blue light, and prefers green light to red light at different times of the daily 24-hour cycle. The authors also pinpoint separate mechanisms for these behavioural responses.

Light influences various behaviours in insects, and fruit flies serve as a model in which to study the mechanisms underlying this effect. Flies avoid or are attracted to light depending on its intensity and colour and the duration and time of day of the exposure5,6. However, it is unclear whether fruit flies have intrinsic colour preferences, as do primates7 and, if so, how these preferences are mediated.

Lazopulo et al. analysed video recordings of the position and movements of individual flies living in glass tubes, each of which contained three equally sized zones that were covered by blue, green or red filters. The authors placed food at one end of each tube, and varied the order of the coloured zones along the tubes to avoid misinterpreting flies’ preference for the zone that contained food as reflecting a colour preference. To simulate the day–night cycle, the flies were kept in light–dark conditions (12 hours of light and 12 hours of darkness), and thus the colours were visible only during the light phase. Consistent with this, the flies showed no preference for any particular coloured part of the tube during the dark phase.

During the light phase, however, the flies exhibited a complex, systematic pattern of colour preference (Fig. 1). They consistently avoided the blue-light zone; furthermore, they spent more time in the green zone than in the red zone in the early morning and late afternoon, when the flies showed bursts of activity8. Such timed preferences are intuitively advantageous, because some of this activity is devoted to searching for food, and flies often find food in or under green trees and bushes.

Figure 1 | Flies show differences in colour preference during the day. Lazopulo et al.4 assessed the colour preferences of fruit flies (Drosophila) at various times of day as they moved freely between three differently coloured zones — blue, red and green — of glass tubes. a, Wild-type flies showed no preference for any of the three zones during the 12-hour dark period. But, during the light phase, they avoided the blue zone and preferred the green zone to the red zone during their morning and evening activity bouts. b, Flies that were genetically engineered to lack a 24-hour biological rhythm (clock-gene mutants) preferred green light to red light across the whole light phase. c, By contrast, flies that expressed less of a light-sensitive pigment called rhodopsin 1 in their eyes than normal flies did not prefer green light to red light (which flies perceive as dim light). d, Unexpectedly, flies that expressed less-than-normal levels of another rhodopsin pigment, rhodopsin 7, in pain-sensitive neuronal cells in the body wall did not avoid blue light.

Flies lack photoreceptors (light-sensitive cells) that are specifically sensitive to red light, although their green-light photoreceptors show some sensitivity to red light9; thus, they probably experience the red light as dim green light or just dim light. Lazopulo et al. observed that the flies tended to rest under red or green light during their midday ‘siesta’ (Fig. 1). However, when they could choose between bright green light and dim white light, the flies generally chose to have their siesta in dim white light. These results suggest that flies prefer to rest under dim light.

Nonetheless, when the flies could choose between bright green and dim blue light for their siesta, the flies always preferred green. This implies that flies decide between green and blue on the basis of colour (wavelength) of the light, rather than intensity. Indeed, their strong aversion to blue light during the siesta makes sense because blue light (and ultraviolet light, which has a slightly shorter wavelength and higher energy) can damage DNA and can therefore be harmful10.

Light-activated pigments called rhodopsins are expressed by photoreceptor cells in the eyes of animals. The authors monitored the colour preferences of fly strains that were genetically engineered to have mutations in genes expressed by photoreceptor cells, including those encoding rhodopsins. They found that rhodopsin 1, which is the most abundant rhodopsin expressed in the compound eyes of fruit flies, is necessary for green-light preference, whereas rhodopsin 6 contributes to the preference for dim light during siesta time. Both rhodopsins are more sensitive to green light than to other colours, and photoreceptor cells that express these rhodopsins signal to a group of neuronal cells in the brain — known as the central clock11 that regulate many biological processes over the 24-hour (circadian) period. Thus, the central clock might time the changes in green-light preference.

‘Clock’ genes expressed by neurons in the central clock interact with one another in a complex feedback loop that serves as a timekeeping mechanism. The authors tested clock-gene mutants12 whose genetic clock did not function, or ran faster or slower than normal. Flies that lacked a functioning clock did not show morning and evening peaks in green-light preference and instead preferred green light throughout the entire light period. By contrast, mutants whose internal clocks ran faster or slower than normal had an abnormally timed preference to green light. Notably, however, the clock-gene mutants still avoided blue light, indicating that this behaviour does not require a functional circadian clock.

Unexpectedly, the authors established that the photoreceptor cells responsible for blue-light avoidance are not located in the head; neither the compound eyes, nor the blue-light-sensitive protein cryptochrome, which is present in the circadian clock neurons, were needed for this response. Instead, rhodopsin 7, expressed by pain-sensing neurons of the body wall, was required for blue-light avoidance. These neurons mediate escape responses of the fly to high temperatures, potentially harmful chemicals and mechanical stimuli. Rhodopsin 7 is present at low levels in several fly tissues, and its sensitivity to ultraviolet and blue light was characterized only a few years ago13,14. Its function has been debated, but Lazopulo et al. seem to have found a crucial function of rhodopsin 7.

The study shows for the first time that pain-sensing neurons in the body wall of adult flies can detect light and mediate consistent avoidance of short-wavelength light. Until now, this had been reported only in larvae15. Previous studies measured adult flies’ colour preferences by placing them between two tubes lit with different colours (generally UV, green or blue)5,16,17. Depending on the available choice, the flies moved towards UV or blue light. By contrast, the flies in Lazopulo and colleagues’ study were not attracted to blue or UV light at any time of the day.

This difference in result is probably due to the fact that in the Lazopulo et al. experimental set-up, the flies could freely choose a preferred place, completely undisturbed. In previous studies, flies were aroused either by being placed together in a new environment5,16,17 or by acute exposure to light6 before they could choose between different colours. Therefore, these previous experiments measured phototactic responses — that is, movements towards or away from a light source — rather than intrinsic preferences for certain colours. Phototactic responses depend on the function of the flies’ eyes5,6,16,17. Thus, the mechanisms that control phototactic behaviour and the avoidance of blue light are distinct.

It remains to be seen how the two pathways that control the preference for green light and the avoidance of blue light work together in fruit flies. Lazopulo and colleagues’ findings also raise the question of how other animals, including mammals, respond to different colours at different times of day, and whether similar pathways exist in other animals. Rhodopsin 7 is present in most arthropods18 (joint-legged invertebrates) and might have a similar role in these animals. However, it is absent in vertebrates, and humans don’t seem to have a sensor in their skin that enables them to avoid blue light. If they did, they probably wouldn’t spend hours in the sun getting a tan.

Nature 574, 43-44 (2019)

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