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

Abstract

Frolov R, Weckström M. Developmental changes in biophysical properties of photoreceptors in the common water strider (Gerris lacustris): better performance at higher cost. J Neurophysiol 112: 913-922, 2014. First published May 28, 2014 doi:10.1152/jn.00239.2014.-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 Ϯ 20 vs. 43 Ϯ 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 ϩ (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 ϩ 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 ϳ7.6-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.Gerris lacustris; water strider; photoreceptor; ion channels; photoreceptor development CHANGES IN BIOPHYSICAL PROPERTIES and signaling of photoreceptors during postembryonic growth are poorly studied and understood in insects with incomplete metamorphosis. After insects hatched from the egg, the eyes, retina, and photoreceptors may undergo rapid growth (Keskinen and Meyer-Rochow 2004;Meyer-Rochow and Keskinen 2003;Stark and Mote 1981), with changes in the total membrane area, rhabdom size, and ion channel composition of photoreceptors. These changes, in turn, alter electrical properties of photoreceptors such as resting potential, rectification, and membrane filtering. A major point of interest here is how these developmental changes in photoreceptor function accommodate behavioral challenges imposed by the growing animal's visual ecology, which may be quite differe...

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

“…may also positively or negatively correlate with photoreceptor size, which might explain why we have consistently observed strong correlations between these two photoreceptor properties in different insect species. In this regard, it is interesting that in all species presented in figure 6, the variations in sensitivity are similarly proportional to the variations in capacitance: if we quantify each correlation by first obtaining the interquartile ranges for both sensitivity and capacitance, and then divide the interquartile range for absolute sensitivity by that for the capacitance variation, the resulting ratios are similar: 0.0072 for the cockroach, 0.0088 for the backswimmer, 0.0092 for the stick insect and 0.0139 for the water strider (although in the latter case there were two classes of peripheral photoreceptors, blue and green, characterized by different absolute sensitivities and average capacitances) [31].…”

“…Importantly, all these species have different visual ecologies: the stick insect Carausius morosus is strictly nocturnal, the water strider Gerris lacustris is strictly diurnal, and the American cockroach Periplaneta americana is active during twilight and night-time. All these species demonstrate strong positive correlations between absolute sensitivity and capacitance [28,31] (P. americana sensitivity and capacitance values were obtained from the dataset as published by Immonen et al [40]). In fact, this was found in all insect species where we addressed this issue, without exception.…”

“…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.…”

Static and Dynamic Adaptation of Insect Photoreceptor Responses to Naturalistic Stimuli

“…Adult backswimmers ( Notonecta glauca ) were collected locally in Oulu (Finland) or purchased from Blades Biological Ltd. Photoreceptors were always allowed to adapt to dark conditions for periods of several minutes before recordings. Some recordings from N. glauca and G. bimaculatus were used previously (Frolov and Weckström, 2014; Immonen et al, 2014a). Ommatidia were dissociated as described previously (Krause et al, 2008; Immonen et al, 2014b).…”

Visual ecology and potassium conductances of insect photoreceptors

“…The data in Table 1 show that A. mellifera, C. vicina, and P. xuthus are highly visual, strictly diurnal, fast-flying insects with large apposition eyes, small interommatidial angles with less than 1°in zones of highest acuity (Land 1997), and prominent visually guided behavior in general and with regard to rapid in-air maneuvering and escape reactions. In contrast, D. melanogaster, though displaying impressive aerobatics (Dubnau 2014;Fry et al 2003), is a relatively slow flier, which received a zero score for the "flight" category. It should be noted that although small insects usually cannot fly fast, D. melanogaster seems to fly slower than hematophagic insects of similar or even smaller size, such as black flies (e.g., Simuliidae) and biting midges (e.g., Ceratopogonidae).…”