Color vision in insects: insights from Drosophila

Abstract

Color vision is an important sensory capability that enhances the detection of contrast in retinal images. Monochromatic animals exclusively detect temporal and spatial changes in luminance, whereas two or more types of photoreceptors and neuronal circuitries for the comparison of their responses enable animals to differentiate spectral information independent of intensity. Much of what we know about the cellular and physiological mechanisms underlying color vision comes from research on vertebrates including primates. In insects, many important discoveries have been made, but direct insights into the physiology and circuit implementation of color vision are still limited. Recent advances in Drosophila systems neuroscience suggest that a complete insect color vision circuitry, from photoreceptors to behavior, including all elements and computations, can be revealed in future. Here, we review fundamental concepts in color vision alongside our current understanding of the neuronal basis of color vision in Drosophila, including side views to selected other insects.

Keywords: Color opponency; Photoreceptor; Rhodopsin; Spectral processing; Wavelength discrimination.

Fig. 1

Color vision facilitates image segmentation, object identification, and underlies diverse behaviors. a Addition of spectral contrast to the black and white image facilitates the segregation of objects from background. Field cow-wheat (Melampyrum arvense) pops out from the meadow when displayed in color. b Color vision enables a more accurate judgement of the properties of objects. For instance, floral color change can provide important cues for pollinators. After opening when flowers are still loaded with nectar, the shown Lantana (Lantana camara) flowers are yellowish. They change to orange and purple-red when nectar is increasingly depleted (Weiss 1991). c Color vision can enable intraspecific communication, also in the presence of co-occurring mimics. The wing patterns of Heliconius (Heliconius numata, upper left) and several closely related genera (Eueides isabella, lower right) display a shared warning signal. Yellow pigmentation in Heliconius numata with additional reflection in the UV, and additional UV sensitivity are consistent with a trait for intraspecific communication (Bybee et al. 2012). d Color vision can enable the detection of wing interference patterns (WIPs) that are displayed by the wings of most Hymenoptera and Diptera (here Drosophila melanogaster). WIPs have been suggested to serve intraspecific communication and were recently shown to be an important trait in sexual selection behavior in Drosophila (Shevtsova et al. ; Hawkes et al. 2019). e Insect color vision with sensitivity in the UV range of the spectrum, in addition to sensitivity for longer wavelengths, allows many insects to detect patterns on flowers that are hidden to the human eye. A buttercup flower (Caltha palustris) is perceived homogeneous yellow by a human observer (left) although it strongly reflects in the UV range (right, photographed with a 310–390 nm filter and displayed in greyscale). Images in (c) modified, Bybee et al. (d) Shevtsova et al. ; (e) modified, © Dr Schmitt, Weinheim Germany, uvir.eu

Fig. 2

Photoreceptor functions, color opponent processing and photoreceptor sensitivity in selected insects. a, a′ Principle of univariance: light stimuli S1, S2, and S3 differ in wavelength and intensity (a), but elicit identical responses in a given photoreceptor (a´). b Example for a dichromatic color vision system with short and long wavelength-sensitive photoreceptors. b′ The metameric light stimuli (S₁ + S_1*) and S₂ elicit same response in the two types of photoreceptors and are therefore interpreted as same color. c Neuronal response of a hypothetic color opponent neuron that receives antagonistic input from the two types of photoreceptors in (b). d Spectral sensitivities of the three types of photoreceptors in the trichromatic honey bee visual system (peak sensitivity in the UV, blue, and green range of the spectrum). e Spectral sensitivities of the five types of rhodopsins expressed in the predominating types of photoreceptors of the Drosophila eye (maximum sensitivity at 478 nm (Rh1, gray), 345 nm (Rh3, light purple), 375 nm (Rh4, violet), 437 nm (Rh5, blue), or 508 nm (Rh6, green). An accessory pigment mediates additional UV sensitivity in R1–R6. f Spectral sensitivities of the six classes of spectral receptors of Papilio xuthus: UV, violet, blue, green (double-green depicted), red and broad-band. Images modified, after (d) Osorio and Vorobyev (2008); (e) Salcedo et al. (1999) and Schnaitmann et al. (2018), and (f) Arikawa (2017)

Fig. 3

Schematic representation of photoreceptor composition in the predominating types of ommatidia in the Drosophila, honey bee, and butterfly (Papilio xuthus) eye. a In Drosophila, rhodopsin expression in the long visual fibers (lvfs) R7/R8 differs in yellow (y), dorsal-yellow (dy, in the dorsal third retina), and pale (p) ommatidia. R7p/R8p express rh3/rh4 (light purple/blue), R7y/R8y express rh4/rh6 (dark purple/green), and dy R8/R7 express rh6 and rh3 + rh4. Short visual fibers (svfs) R1–R6 homogeneously express rh1 (Salcedo et al. 1999). b In Apis mellifera, opsin expression in the two lvfs determines three main ommatidia types. In type I, one lvf expresses UV sensitive (light purple), the other blue (blue) sensitive opsin. Both lvfs express UV sensitive opsin in type II, and blue sensitive opsin in type III ommatidia. Short visual fibers uniformly express green sensitive opsin in all ommatidia. The sensitivity and function of the small R9 is unknown (Wakakuwa et al. 2005). c In Papilio xuthus, UV and blue sensitive opsin expression in the lvfs of type I–III ommatidia is similar as in bees. In all ommatidia types, two svfs co-express two long wavelength-sensitive opsins providing them with maximum sensitivity to green light. The remaining four svfs express red sensitive opsin in type I, red plus green sensitive opsins in type II, and green sensitive opsin in III. Furthermore, spectral sensitivity of Papilio photoreceptors is modulated by red (type I and II) or yellow (type III) perirhabdomal pigments and ‘fluorescence pigment’ (type II) (Arikawa 2017). The sensitivity of small R9 is unknown. In the neuronal superposition eye of Drosophila, the individual rhabdomeres (gray in a) are spatially and optically separated. In contrast, bee and butterfly ommatidia have a so-called fused rhabdom, where the light-sensitive structures of the individual photoreceptors are grouped closely together and acts as a light guide

Fig. 4

Neuronal basis of color vision in Drosophila. a Anatomical representation of demonstrated and candidate color processing neurons in the fly optic lobe. Retina (Re), lamina (La), medulla (Me), lobula (Lo), and lobula plate (Lop). b R7 and R8 photoreceptors of the same type of ommatidia mutually inhibit each other directly via HisCl1 histamine receptors and receive additional feedback inhibition via Dm9 that requires the second histamine receptor Ort (Schnaitmann et al. ; manuscript in preparation). c Connectivity and suggested function of the cells in (a). The axons of R7 and R8 pass through the lamina and convey information to the distal layers m1–m6 of the medulla. Transmedulla neurons Tm5a, b, c and Tm20, but also amacrine cells including Dm8 receive direct input from R7 or R8. R7 and R8 terminals mutually inhibit each other [see (b)]. The svfs of the outer photoreceptors R1–R6 convey information to the lamina monopolar cells L1–L3 that in turn project to the medulla. Simultaneous block of L1 and L2 prohibited blue–green discrimination in a memory task (Schnaitmann et al. 2013). L1–L3 connect to a range of different Tms, among them some with a function in color vision (Tm20 for L2 and L3, Tm5a for L3) (Gao et al. ; Takemura et al. 2015). Tm5a,b,c, and Tm20 establish redundant channels of the color vision system (Melnattur et al. 2014). The R7 → Dm8 → Tm5c pathway and the medulla columnar neuron MC61 are necessary for UV/green preference behavior (Gao et al. ; Otsuna et al. ; Karuppudurai et al. 2014). Tms relay information to the Lobula, for instance, to the lobula intrinsic neuron Li4 and the visual projection neuron LT11 (not shown, Otsuna et al. ; Lin et al. 2016). VPN–MB1 establish a direct link from the medulla to the mushroom body, and are necessary for color discrimination in a memory task (Vogt et al. 2016). Round endings and arrowheads denote inhibitory (histamine) and excitatory connections, respectively. Dashed lines indicate unspecified connectivity. Image in (a) after Fischbach and Dittrich (1989)