The pigment transporter Redboy confers programmed body colour transition in orchid mantises

Programmed phenotypic transition is prevalent throughout the tree of life, yet the concrete mechanisms that underpin this phenomenon are poorly understood. The orchid mantis (Hymenopus coronatus, Mantodea) is a model study system for programmed body colour transitions that displays a prominent black-red body colour in first-instar nymphs, then switches to a flowery white body colour in later-instar nymphs. Here we reveal that this body colour transition is achieved by the simultaneous excretion of decarboxylated-xanthommatin (red pigment) and the accumulation of uric acid (white pigment) in the epidermis during the first moult. This change in pigmentation is associated with a novel subtype of ABCG pigment transporter that we call 'Redboy' in Polyneoptera, which is upregulated by insect steroid hormone (ecdysone) during the first moult of orchid mantises. RNAi assay and pigment analyses show that Redboy functions together with the co-transporter White, exporting red pigments from and concurrently importing white pigments into the epidermal cells. Spectral reflectance analyses and predation experiments reveal that Redboy-conferred programmed body colour transition enhances predator avoidance during the first instar, and both prey attraction and predator avoidance in later instars. Our findings clarify how gene family evolution and hormone regulation coordinate programmed phenotypic transition and promote ecological adaptation in orchid mantises.