Developmental changes in biophysical properties of photoreceptors in the common water strider (Gerris lacustris): better performance at higher cost

Although the dependence of invertebrate photoreceptor biophysical properties on visual ecology has already been investigated in some cases, developmental aspects have largely been ignored due to the general research emphasis on holometabolous insects. Here, using the patch-clamp method, we examined changes in biophysical properties and performance of photoreceptors in the common water strider Gerris lacustris during postembryonic development. We identified two types of peripheral photoreceptors, green and blue sensitive. Whole cell capacitance (a measure of cell size) of blue photoreceptors was significantly higher than the capacitance of green photoreceptors (69 +/- 20 vs. 43 +/- 12 pF, respectively). Most of the measured morphological and biophysical parameters changed with development. Photoreceptor capacitance increased progressively and was positively correlated with sensitivity to light, magnitudes and densities of light-induced (LIC) and delayed rectifier K+ (I-DR) currents, membrane corner frequency, and maximal information rate [ Spearman rank correlation coefficients: 0.70 (sensitivity), 0.79 (LIC magnitude), 0.79 (I-DR magnitude), 0.48 (corner frequency), and 0.57 (information rate)]. Transient K+ current increased to a smaller extent, while its density decreased. We found no significant changes in the properties of single photon responses or levels of light-induced depolarization, the latter indicating a balanced channelome expansion associated with I-DR expression. However, the dramatic similar to 7.6-fold increase in I-DR from first instars to adults indicated a development-related rise in the metabolic cost of information. In conclusion, this study provides novel insights into functional photoreceptor adaptations with development and illustrates remarkable variability in patterns of postembryonic retinal development in hemimetabolous insects with dissimilar visual ecologies and behaviors.