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 ϩ current did not increase but the delayed rectifier doubled in adults compared with nymphs, the K ϩ 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 Ϯ 0.7 bits/s versus 34.1 Ϯ 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.

Biophysical properties of photoreceptors in Corixa punctata facilitate diurnal life-style

“…At even higher light intensities photoreceptor performance deteriorated, clearly due to saturation of phototransduction units in dissociated ommatidia illuminated side-on and deprived of optical adaptation mechanisms (Howard, Blakeslee, & Laughlin, 1987;Song et al, 2012). These observations are consistent with findings in other insect species studied with the patch-clamp method Frolov et al, 2012;Immonen, Ignatova, et al, 2014). The maximal average IR (IR max ) was 36.0 ± 21.3 bits s À1 with the f 3dB of 5.6 ± 0.3 Hz (n = 14).…”

“…3B emphasizes differences in absolute sensitivity distributions between these species. These data were obtained in previous studies using the same experimental procedures Frolov et al, 2012;Immonen, Ignatova, et al, 2014;Immonen, Krause, et al, 2014) (for photoreceptors with peak spectral sensitivities wavelengths other than 525 nm, the absolute sensitivity values were adjusted to match the photon flux at 525 nm). The maximal steady-state LIC (LIC ss ), which was determined as the LIC at 2 s after the onset of light following photoreceptor stimulation with increasingly bright constant-light stimuli, correlated …”

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

“…In vitro absolute sensitivity in species with different visual ecologies. Correlations between absolute sensitivity and capacitance are shown for four insects: N. glauca, the stick insect C. morosus [28], the water strider G. lacustris [31] and the American cockroach P. americana; data are presented for adult specimens only; in the case of P. americana, the same dataset was used to extract sensitivity values as published by Immonen et al [40]. Data are presented in terms of bumps s 21 at the light level corresponding to the level -7 in figure 1d. rspb.royalsocietypublishing.org Proc.…”

“…Dissociation of ommatidia (electronic supplementary material, figure S1) and electrophysiological recordings were performed as described previously [26][27][28] …”

“…Light stimulation was performed as described previously [28]. In brief, a computer-controlled custom-made voltage-to-current driver for light-emitting diodes (LEDs) was used to drive 10 (in patch-clamp experiments) or 13 (in intracellular experiments) monochromatic LEDs (Roithner Laser Technik, Austria), covering a range from 355 to 639 nm, which were used in combination with neutral density filters (Kodak, New York, NY, USA).…”