In fly photoreceptors, light is focused onto a photosensitive waveguide, the rhabdomere, consisting of tens of thousands of microvilli. Each microvillus is capable of generating elementary responses, quantum bumps, in response to single photons using a stochastically operating phototransduction cascade. Whereas much is known about the cascade reactions, less is known about how the concerted action of the microvilli population encodes light changes into neural information and how the ultrastructure and biochemical machinery of photoreceptors of flies and other insects evolved in relation to the information sampling and processing they perform. We generated biophysically realistic fly photoreceptor models, which accurately simulate the encoding of visual information. By comparing stochastic simulations with single cell recordings from Drosophila photoreceptors, we show how adaptive sampling by 30,000 microvilli captures the temporal structure of natural contrast changes. Following each bump, individual microvilli are rendered briefly (~100-200 ms) refractory, thereby reducing quantum efficiency with increasing intensity. The refractory period opposes saturation, dynamically and stochastically adjusting availability of microvilli (bump production rate: sample rate), whereas intracellular calcium and voltage adapt bump amplitude and waveform (sample size). These adapting sampling principles result in robust encoding of natural light changes, which both approximates perceptual contrast constancy and enhances novel events under different light conditions, and predict information processing across a range of species with different visual ecologies. These results clarify why fly photoreceptors are structured the way they are and function as they do, linking sensory information to sensory evolution and revealing benefits of stochasticity for neural information processing.

The compound eye of insects imposes a tradeoff between resolution and sensitivity, which should exacerbate with diminishing eye size. Tiny lenses are thought to deliver poor acuity because of diffraction; nevertheless, miniature insects have visual systems that allow a myriad of lifestyles. Here, we investigate whether size constraints result in an archetypal eye design shared between miniature dipterans by comparing the visual performance of the fruit fly Drosophila and the killer fly Coenosia. These closely related species have neural superposition eyes and similar body lengths (3 to 4 mm), but Coenosia is a diurnal aerial predator, whereas slow-flying Drosophila is most active at dawn and dusk. Using in vivo intracellular recordings and EM, we report unique adaptations in the form and function of their photoreceptors that are reflective of their distinct lifestyles. We find that although these species have similar lenses and optical properties, Coenosia photoreceptors have three- to fourfold higher spatial resolution and rate of information transfer than Drosophila. The higher performance in Coenosia mostly results from dramatically diminished light sensors, or rhabdomeres, which reduce pixel size and optical cross-talk between photoreceptors and incorporate accelerated phototransduction reactions. Furthermore, we identify local specializations in the Coenosia eye, consistent with an acute zone and its predatory lifestyle. These results demonstrate how the flexible architecture of miniature compound eyes can evolve to match information processing with ecological demands.