Abstract
Light sensing by tissues distinct from the eye occurs in diverse animal groups, enabling circadian control and phototactic behaviour. Extraocular photoreceptors may also facilitate rapid colour change in cephalopods and lizards, but little is known about the sensory system that mediates slow colour change in arthropods. We previously reported that slow colour change in twig-mimicking caterpillars of the peppered moth (Biston betularia) is a response to achromatic and chromatic visual cues. Here we show that the perception of these cues, and the resulting phenotypic responses, does not require ocular vision. Caterpillars with completely obscured ocelli remained capable of enhancing their crypsis by changing colour and choosing to rest on colour-matching twigs. A suite of visual genes, expressed across the larval integument, likely plays a key role in the mechanism. To our knowledge, this is the first evidence that extraocular colour sensing can mediate pigment-based colour change and behaviour in an arthropod.
Highlights
Background choiceTo further evaluate the capacity of B. betularia caterpillars for extraocular colour perception, we tested background choice behaviour using two designs of background choice arena: a transparent plastic cube containing two diagonally crossing dowels, each painted with a single colour; and a transparent horizontal tube with a single horizontally suspended dowel, one half painted green, and the other brown
B. betularia larvae reared in white dowel enclosures were significantly brighter than those reared on black dowels, when measured as the double cone responses of the avian retina (F1,127 = 177.4, P < 0.0001; Fig. 2b), but there was no significant effect of blindfolding on the luminance of larvae from black or white treatments (F1,127 = 0.28, P = 0.6)
Biston betularia larvae that were prevented from receiving light input through their ocelli changed colour in response to luminance and colour cues, and maximised the benefits of this plastic masquerade by actively selecting twigs of similar colour
Summary
To further evaluate the capacity of B. betularia caterpillars for extraocular colour perception, we tested background choice behaviour using two designs of background choice arena: a transparent plastic cube containing two diagonally crossing dowels, each painted with a single colour (bright green vs dark brown); and a transparent horizontal tube with a single horizontally suspended dowel, one half painted green, and the other brown (see ‘Methods’). These two designs allowed us to test a b c Reflectance (%) Luminance. We determined the coding sequence (CDS) for visual arrestin-1
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