Color vision is widespread among insects but varies among species, depending on the spectral sensitivities and interplay of the participating photoreceptors. The spectral sensitivity of a photoreceptor is principally determined by the absorption spectrum of the expressed visual pigment, but it can be modified by various optical and electrophysiological factors. For example, screening and filtering pigments, rhabdom waveguide properties, retinal structure, and neural processing all influence the perceived color signal. We review the diversity in compound eye structure, visual pigments, photoreceptor physiology, and visual ecology of insects. Based on an overview of the current information about the spectral sensitivities of insect photoreceptors, covering 221 species in 13 insect orders, we discuss the evolution of color vision and highlight present knowledge gaps and promising future research directions in the field.

The ventral compound eye of many insects contains polarization-sensitive photoreceptors, but little is known about how they are integrated into visual functions. In female horseflies, polarized reflections from animal fur are a key stimulus for host detection. To understand how polarization vision is mediated by the ventral compound eye, we investigated the band-eyed brown horsefly Tabanus bromius using anatomical, physiological, and behavioral approaches. Serial electron microscopic sectioning of the retina and single-cell recordings were used to determine the spectral and polarization sensitivity (PS) of photoreceptors. We found 2 stochastically distributed subtypes of ommatidia, analogous to pale and yellow of other flies. Importantly, the pale analog contains an orthogonal analyzer receptor pair with high PS, formed by an ultraviolet (UV)-sensitive R7 and a UV- and blue-sensitive R8, while the UV-sensitive R7 and green-sensitive R8 in the yellow analog always have low PS. We tested horsefly polarotaxis in the field, using lures with controlled spectral and polarization composition. Polarized reflections without UV and blue components rendered the lures unattractive, while reflections without the green component increased their attractiveness. This is consistent with polarotaxis being guided by a differential signal from polarization analyzers in the pale analogs, and with an inhibitory role of the yellow analogs. Our results reveal how stochastically distributed sensory units with modality-specific division of labor serve as separate and opposing input channels for visual guidance.

The visual system of the European corn borer (ECB, Ostrinia nubilalis) was analysed with microscopy and electrophysiological methods (ERG, single cell recordings). The ECB has a pair of mainly ultraviolet-sensitive ocelli and a pair of compound eyes, maximally sensitive to green light. The ommatidia contain a tiered, fused rhabdom, consisting of the rhabdomeres of 9-12 photoreceptor cells with sensitivity peak wavelengths at 356, 413, 480, and 530 nm. The photoreceptors in a large dorsal rim area have straight rhabdomeres and high polarization sensitivity (PS1,2=3.4, 14). Elsewhere, in the main retina, the majority of photoreceptors have non-aligned microvilli and negligible PS, but each ommatidium contains one or two blue-sensitive distal photoreceptors with straight microvilli parallel to the dorsoventral axis, yielding extremely high PS (PS1,2,3=56, 63, 316). Rhabdoms containing distal cells with potentially high PS have evolved at least two times, in moths (Crambidae, Noctuidae, Saturniidae) as well as in dung beetles (Scarabaeidae). The distal photoreceptors with high PS, sensitive to vertically polarized light, represent a monopolatic system which is unsuitable for the proper analysis of e-vector orientation. Anyhow, the distal photoreceptors might be used in conjunction with polarization-insensitive photoreceptors to detect objects that reflect polarized light with stereotyped orientation.

The butterflyPapilio xuthushas acute tetrachromatic color vision. Its eyes are furnished with eight spectral classes of photoreceptors, situated in three types of ommatidia, randomly distributed in the retinal mosaic. Here, we investigated early chromatic information processing by recording spectral, angular, and polarization sensitivities of photoreceptors and lamina monopolar cells (LMCs). We identified three spectral classes of LMCs whose spectral sensitivities corresponded to weighted linear sums of the spectral sensitivities of the photoreceptors present in the three ommatidial types. In ~ 25% of the photoreceptor axons, the spectral sensitivities differed from those recorded at the photoreceptor cell bodies. These axons showed spectral opponency, most likely mediated by chloride ion currents through histaminergic interphotoreceptor synapses. The opponency was most prominent in the processes of the long visual fibers in the medulla. We recalculated the wavelength discrimination function using the noise-limited opponency model to reflect the new spectral sensitivity data and found that it matched well with the behaviorally determined function. Our results reveal opponency at the first stage ofPapilio’s visual system, indicating that spectral information is preprocessed with signals from photoreceptors within each ommatidium in the lamina, before being conveyed downstream by the long visual fibers and the LMCs.

In many butterflies, the ancestral trichromatic insect colour vision, based on UV-, blue- and green-sensitive photoreceptors, is extended with red-sensitive cells. Physiological evidence for red receptors has been missing in nymphalid butterflies, although some species can discriminate red hues well. In eight species from genera Archaeoprepona, Argynnis, Charaxes, Danaus, Melitaea, Morpho, Heliconius and Speyeria , we found a novel class of green-sensitive photoreceptors that have hyperpolarizing responses to stimulation with red light. These green-positive, red-negative (G+R–) cells are allocated to positions R1/2, normally occupied by UV and blue-sensitive cells. Spectral sensitivity, polarization sensitivity and temporal dynamics suggest that the red opponent units (R–) are the basal photoreceptors R9, interacting with R1/2 in the same ommatidia via direct inhibitory synapses. We found the G+R– cells exclusively in butterflies with red-shining ommatidia, which contain longitudinal screening pigments. The implementation of the red colour channel with R9 is different from pierid and papilionid butterflies, where cells R5–8 are the red receptors. The nymphalid red-green opponent channel and the potential for tetrachromacy seem to have been switched on several times during evolution, balancing between the cost of neural processing and the value of extended colour information.