The eyes and vision of butterflies

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Abstract

Butterflies use colour vision when searching for flowers. Unlike the trichromatic retinas of humans (blue, green and red cones; plus rods) and honeybees (ultraviolet, blue and green photoreceptors), butterfly retinas typically have six or more photoreceptor classes with distinct spectral sensitivities. The eyes of the Japanese yellow swallowtail (Papilio xuthus) contain ultraviolet, violet, blue, green, red and broad-band receptors, with each ommatidium housing nine photoreceptor cells in one of three fixed combinations. The Papilio eye is thus a random patchwork of three types of spectrally heterogeneous ommatidia. To determine whether Papilio use all of their receptors to see colours, we measured their ability to discriminate monochromatic lights of slightly different wavelengths. We found that Papilio can detect differences as small as 1–2 nm in three wavelength regions, rivalling human performance. We then used mathematical modelling to infer which photoreceptors are involved in wavelength discrimination. Our simulation indicated that the Papilio vision is tetrachromatic, employing the ultraviolet, blue, green and red receptors. The random array of three ommatidial types is a common feature in butterflies. To address the question of how the spectrally complex eyes of butterflies evolved, we studied their developmental process. We have found that the development of butterfly eyes shares its molecular logic with that of Drosophila: the three-way stochastic expression pattern of the transcription factor Spineless determines the fate of ommatidia, creating the random array in Papilio.

The Japanese yellow swallowtail butterfly, Papilio xuthus, a model insect species for studying colour vision. Colour vision properties of Papilio have been extensively studied by psychophysical methods. A, a female taking nectar on Zinnia sp. B, head of a pupa whose spineless gene was knocked out by a gene-editing technique CRISPR-Cas9. Bilateral antennae were not formed normally (black arrowhead). White arrowhead indicates the eye disc. C, head of a Spineless-knockout adult. The antennae did not extend (black arrowhead), and the spectral organization of the compound eye was modified as well.

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