title: Extraocular photoreception and colour plasticity in caterpillars of the peppered moth, Biston betularia
Creators: name: Eacock, A
Publisher: name: University of Liverpool Repository
Year: 2018

description: Visual camouflage is a textbook example of natural selection, and a widespread strategy used by both predators and prey to avoid detection. Background matching, where the animal resembles the colour, brightness, and/ or pattern of the surrounding visual background is a common form of visual camouflage, and can occur through genetic polymorphism, behavioural background choice, or dynamic colour change. Dynamic colour change can occur very rapidly (milliseconds) or gradually, sometimes taking weeks to complete. Visual cues such as colour, brightness, and pattern, have been shown to elicit colour change, and in some colour-changing animals visual cues are sensed outside of the eye using extraocular photoreceptors (EOPs). Colour change research has been focused predominantly on rapid, chromatophore-based colour change, as observed in cephalopods. In contrast, little is known about the physiology and evolutionary origins of gradual colour change. To avoid predation in a wide range of environments, caterpillars of the peppered moth (Biston betularia) masquerade as twigs and gradually change colour to match them. This thesis investigates the colour-changing response in B. betularia larvae: the shape of the reaction norm to colour and brightness gradients; the use and molecular basis of extraocular photoreception; and whether B. betularia alter resting behaviour to maximise concealment. Through a series of artificial twig experiments, I found that B. betularia larvae respond to both colour and luminance cues to produce a continuous range of phenotypes, rather than being restricted to a brown/green polyphenism as previously reported. To test for the possibility of extraocular photoreception, I occluded the eyes (ocelli) of groups of larvae and compared responses to colour and luminance with non-blindfolded control larvae. There was no difference in the colour-changing response of blindfolded larvae compared to controls, and blindfolded larvae also rested on colours that better matched their own colour to the same extent as non-blindfolded controls. I next examined the potential for visual machinery in the larval dermis, finding expression of a suite of visual genes throughout dermal tissue in B. betularia larvae and adults. In larvae, this expression was generally much higher relative to head tissue than found for adults. This finding corroborates the morphological and behavioural evidence for dermal photoreceptors in B. betularia larvae. The final chapter is an attempt to examine the exclusivity of extraocular photoreception in B. betularia, and its evolutionary origins, through tissue-specific measurement of opsin expression in larvae and adults of a phylogenetically broad sample of Lepidoptera. Dermal opsin expression was found in other species, but depended on the gene (UV, blue, LW1, LW2) and developmental stage. Phylogenetic signal was found only for expression of LW1 in larvae, and LW2 in adults. Larval colouration strategy between species also appears to affect dermal opsin expression. The thesis provides strong evidence for a novel physiological phenomenon: extraocular colour photoreception in the dermis of an insect, used to mediate colour change and behavioural background choice. The observation that dermal opsin expression occurs in several other species suggests that EOPs may be widespread in the Lepidoptera. Future work should be directed at the challenging task of understanding the mechanism underlying this class of EOPs, and characterising their functional roles in other species.