Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands

Abstract

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.

Fig. 1.

Comparing Coenosia attenuata and Drosophila melanogaster sizes. (A and B) Coenosia ♀ and ♂, respectively, with Drosophila prey, previously caught midflight (Movie S1). (C–E) Anterior-dorsal scanning EM views from heads of Drosophila and Coenosia ♀ and ♂, respectively. The eye of Coenosia is larger than that of Drosophila and contains more ommatidia. (Scales bars, 250 μm.)

Fig. 2.

Lens diameter (D) and interommatidial angle (Δφ) across the eyes (miniature figures to the right indicate the sectioning plane used for each graph). (A) Eyes were divided into anterior, lateral, and posterior regions and the respective lens diameters measured from several locations for each region (n = 1 for each genotype). For each location, the mean distance (n = 5) between the center of neighboring lenses is plotted on the x axis, according to their estimated horizontal position. (B) Mean interommatidial angles from horizontal cuts of ♀ Coenosia and Drosophila. Coenosia have the smallest Δφ in the anterior (frontal) region (Δφ = 1.88°) (n = 2). (C) Even when the center of the acute zone is not sectioned (Fig. S2A), mean Δφ in Coenosia reach smaller values than Drosophila (n = 2 for each genotype). (Scale bars, 200 μm.)

Fig. 3.

Spatial resolution and TEM micrographs of photoreceptors. (A) Spatial resolution of nearly dark-adapted acceptance angle (Δρ) for Drosophila and Coenosia. Mean angular sensitivity functions of female Drosophila and Coenosia ♀ and ♂ data fitted with Gaussians. For Drosophila Δρ = 8.23°, Coenosia ♀ Δρ = 2.88°, and ♂ Δρ = 2.59°. (B) Cross-sections of the distal ommatidia, just below the photoreceptors caps, in the lateral eye regions. (Scale bars, 2 μm.) (C) R6 rhabdomeres are shown as examples for R1–R6 photoreceptors. Male Coenosia rhabdomeres exhibit a “pyramidal” shape. (Scale bars, 500 nm.) See Table S1 for rhabdomere dimensions. (D) R7 Rhabdomeres are shown. (Scale bars, 500 nm.) See Table S1 for rhabdomere dimensions.

Fig. 4.

Temporal resolution of R1–R6 photoreceptors. (A) Responses of five briefly dark-adapted Coenosia, Calliphora, and Drosophila photoreceptors to a 10-ms saturating light pulse. (B) Normalized impulse responses of five briefly light-adapted photoreceptors to a pseudorandom contrast. (C) SNR of voltage responses to a repeated presentation of bright natural light intensity series. High SNRs (>100) at low frequencies, in which most of the power of natural images resides, implies that signaling is not limited by phototransduction noise. (D) Information transfer of the same responses as in C, calculated as the difference between their entropy and noise entropy (Fig. S3).