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 (Cm), 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 Cm, so that nocturnal species had relatively large and prolonged current bumps. Consequently, although the voltage bump amplitude correlated negatively with Cm, the strength of the total voltage signal increased. Importantly, the background voltage noise decreased strongly with increasing Cm, yielding a notable increase in signal-to-noise ratio for voltage bumps. A similar decrease in the background noise with increasing Cm was found in intracellular recordings in vivo. Morphological measurements of rhabdomeres were consistent with our Cm estimates. Our results indicate that the increased photoreceptor Cm 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