Postembryonic Developmental Changes in Photoreceptors of the Stick InsectCarausius morosus Enhance the Shift to an Adult Nocturnal Life-Style

Abstract

Optimization of sensory processing during development can be studied by using photoreceptors of hemimetabolous insects (with incomplete metamorphosis) as a research model. We have addressed this topic in the stick insect Carausius morosus, where retinal growth after hatching is accompanied by a diurnal-to-nocturnal shift in behavior, by recording from photoreceptors of first instar nymphs and adult animals using the patch-clamp method. In the nymphs, ommatidia were smaller and photoreceptors were on average 15-fold less sensitive to light than in adults. The magnitude of A-type K(+) current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K(+) current densities being greater in the nymphs. By contrast, the density of light-induced current did not increase, although its magnitude increased 8.6-fold, probably due to the growth of microvilli. Nymph photoreceptors performed poorly, demonstrating a peak information rate (IR) of 2.9 ± 0.7 bits/s versus 34.1 ± 5.0 bits/s in adults in response to white-noise stimulation. Strong correlations were found between photoreceptor capacitance (a proxy for cell size) and IR, and between light sensitivity and IR, with larger and more sensitive photoreceptors performing better. In adults, IR peaked at light intensities matching irradiation from the evening sky. Our results indicate that biophysical properties of photoreceptors at each age stage and visual behavior are interdependent and that developmental improvement in photoreceptor performance may facilitate the switch from the diurnal to the safer nocturnal lifestyle. This also has implications for how photoreceptors achieve optimal performance.