Electrophysiological adaptations of insect photoreceptors and their elementary responses to diurnal and nocturnal lifestyles

Abstract

Nocturnal vision in insects depends on the ability to reliably detect scarce photons. Nocturnal insects tend to have intrinsically more sensitive and larger rhabdomeres than diurnal species. However, large rhabdomeres have relatively high membrane capacitance (C m), which can strongly low-pass filter the voltage bumps, widening and attenuating them. To investigate the evolution of photoreceptor signaling under near dark, we recorded elementary current and voltage responses from a number of species in six insect orders. We found that the gain of phototransduction increased with C m , so that nocturnal species had relatively large and prolonged current bumps. Consequently, although the voltage bump amplitude correlated negatively with C m , the strength of the total voltage signal increased. Importantly, the background voltage noise decreased strongly with increasing C m , yielding a notable increase in signal-to-noise ratio for voltage bumps. A similar decrease in the background noise with increasing C m was found in intracellular recordings in vivo. Morphological measurements of rhabdomeres were consistent with our C m estimates. Our results indicate that the increased photoreceptor C m in nocturnal insects is a major sensitivity-boosting and noise-suppressing adaptation. However, by requiring a compensatory increase in the gain of phototransduction, this adaptation comes at the expense of the signaling bandwidth.

Speed of phototransduction in the microvillus regulates the accuracy and bandwidth of the rhabdomeric photoreceptor

“…In contrast, to reliably detect weak light signals in dim light the QB duration increases, at the expense of bandwidth. This is consistent with our previous observations [ 14 ].…”

“…Despite these shortcomings, the proposed method allows reliable determination of median latencies, their scatter, and mean QB half-widths from small voltage impulse responses. This is particularly important in the study of elementary responses of photoreceptors in the fast-flying insect species characterized by very low membrane resistances, small membrane capacitances and small voltage QBs, which cannot be reliably isolated due to large surrounding membrane noise [ 14 ]. An experiment relying on our algorithm could involve stimulation of a dark-adapted photoreceptor with 1 ms or shorter pulses of light of decreasing intensity, until bump-like responses disappear in most of the trials.…”

“…This and the consecutive comparative studies [12][13][14][15] provided insights into the evolution of insect vision, by linking the speed of phototransduction cascade through biophysical properties of the light-insensitive membrane to visual ecology. Thus, in faster diurnal fliers, phototransduction is faster, generates smaller and narrower QBs, and adapts to a greater extent than in slower crepuscular flies.…”

Night skies through animals’ eyes—Quantifying night-time visual scenes and light pollution as viewed by animals

“…Just as when we increase the exposure time for a camera, more photons are thus collected, and a higher signal to noise ratio is achieved ( Snyder, 1977 , 1979 ; Lythgoe, 1979 ; Dubs, 1981 ; Warrant, 1999 ; Laughlin S. B., 1981 ; Warrant and McIntyre, 1996 ). Moreover, integration times tend to be longer in the dark-adapted than the light-adapted state ( Laughlin and Weckström, 1993 ; Juusola and Hardie, 2001 ; Reber et al, 2015 ; Stöckl et al, 2016a ) and also longer in nocturnal than diurnal species ( Laughlin and Weckström, 1993 ; Frederiksen et al, 2008 ; Stöckl A. L. et al, 2017 ; Frolov and Ignatova, 2019 ; Donner, 2021 ). Extremely long integration times have been measured in nocturnal toads [1.5 s ( Donner, 1989 )] and in a deep-sea crustacean [160 ms ( Moeller and Case, 1995 )].…”

Vision does not impact walking performance in Argentine ants

“…Given the relatively slow transduction speeds of walking insect photoreceptors (Frolov et al, 2017), fast movements of the limbs during walking may preclude visual feedback (Full and Koditschek, 1999). Nocturnal and subterranean species particularly confront feedback constraints since transduction speeds depend on both light levels and temperature (Frolov and Ignatova, 2020;Heimonen et al, 2012;Warrant, 2017;Warzecha and Egelhaaf, 2000). These data suggest that vision likely does not influence intra-stride walking coordination but may inform obstacle avoidance at intermediate distances.…”