Graded opsin co-expression along the butterfly retina fine tunes the spectral sensitivity of a colour-opponent cell across the visual field

Compound eyes deliver a vast stream of information to the tiny insect brains. To maximize the information content and minimize the redundancy of neural signals, insect eyes are built so to encode the relevant and filter out the unimportant elements of the visual environment. Terrestrial habitats have a predictable spatio-spectral structure, which can be matched by the distribution of photoreceptors with different spectral sensitivities across the retina. Here, we investigate the retinal organization of the nymphalid butterfly Heliconius melpomene using single-cell recordings, immunohistochemistry and eye shine imaging. The ventral retina is enriched with ommatidia, which contain red screening pigments that shape the spectral sensitivity of basal red receptors R9, while their long visual fibre photoreceptors R1&2, expressing a long-wavelength (L) opsin, are synaptically inhibited by R9 and directly participate in colour vision. These G + R- receptors frequently co-express the L opsin with the blue (B) or ultraviolet (U) opsin. U&L opsin-co-expressing R1&2 are scarce, while B&L co-expression is frequent in the ventral ommatidia and gradually diminishes towards the eye equator, where G + R- receptors express the L opsin only. In this region, G + R- receptors are further inhibited by blue-sensitive receptors. With electrophysiology matching immunohistochemistry, we reveal the fine tuning of spectral sensitivity of a single photoreceptor class across the dorso-ventral axis of the butterfly compound eye. Similar tuning is found in other nymphalid butterflies across the phylogeny, suggesting that this adaptation is ancestral and confers an advantage to those diurnal nymphalids, equipped with the cellular toolkit for colour vision in the red.