Compound Eyes and Retinal Information Processing in Miniature Dipteran Species Match Their Specific Ecological Demands
Total Page：16
File Type：pdf, Size：1020Kb
Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands Paloma T. Gonzalez-Bellidoa,1, Trevor J. Wardilla,1, and Mikko Juusolaa,b,2 aDepartment of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom; and bState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China Edited by Stephen Baccus, University of Miami School of Medicine, Miami, FL, and accepted by the Editorial Board January 10, 2011 (received for review September 28, 2010) The compound eye of insects imposes a tradeoff between formation to detect food and partners, whereas a slow-flying cre- resolution and sensitivity, which should exacerbate with diminish- puscular fructivore may have less urgent demands for its vision. ing eye size. Tiny lenses are thought to deliver poor acuity because Accordingly, compound eyes of many large insects show unique of diffraction; nevertheless, miniature insects have visual systems adaptations; their lens sizes and shapes can vary, including local that allow a myriad of lifestyles. Here, we investigate whether size specializations, such as bright or acute zones for increasing sen- constraints result in an archetypal eye design shared between sitivity or resolution (11), respectively, and their neural responses miniature dipterans by comparing the visual performance of the suggest tuning for the spatial and temporal characteristics of the fruit fly Drosophila and the killer fly Coenosia. These closely re- light environment (12–14). However, given the severity of size lated species have neural superposition eyes and similar body constraints on optics, one is surprised to find a plethora of very Coenosia lengths (3 to 4 mm), but is a diurnal aerial predator, small insects with a vast variety of visually challenging lifestyles. fl Drosophila whereas slow- ying is most active at dawn and dusk. How can their miniature compound eyes allow such richness of Using in vivo intracellular recordings and EM, we report unique visual behaviors? How has their visual information processing adaptations in the form and function of their photoreceptors that fl fi adapted to their different visual lifestyles? NEUROSCIENCE are re ective of their distinct lifestyles. We nd that although We have begun finding answers to these open questions by these species have similar lenses and optical properties, Coenosia investigating the optical and retinal adaptations of two miniature photoreceptors have three- to fourfold higher spatial resolution fl Drosophila. y species with a similar body size and architectural properties and rate of information transfer than The higher per- fl Coenosia (neural superposition eye). The predatory killer y Coenosia formance in mostly results from dramatically diminished fl light sensors, or rhabdomeres, which reduce pixel size and optical attenuata (Muscidae, Coenossinae) and the fruit y Drosophila cross-talk between photoreceptors and incorporate accelerated melanogaster (Drosophilidae, Drosophilinae), which separated phototransduction reactions. Furthermore, we identify local spe- 120 million years ago (15), exhibit specialized behaviors re- fl cializations in the Coenosia eye, consistent with an acute zone and quiring different spatiotemporal visual information. Killer ies fl its predatory lifestyle. These results demonstrate how the flexible can detect a ying prey in the presence of a complex background fl architecture of miniature compound eyes can evolve to match in- and perform a high-speed aerial capture, whereas fruit ies formation processing with ecological demands. distinguish only relatively large and slowly moving objects (16, 17). Using in vivo intracellular recordings, scanning EM, and vision | predatory behavior | invertebrate | evolution transmission EM (TEM), we show that although the lens di- ameter and optical properties are similar in both species, the he design of a compound eye depends on the limits imposed by spatial resolution and information transfer rate of Coenosia Tbody size, architectural properties of the eye, visual task, and photoreceptors are three to four times higher than those of habitat, all of which affect its ability to resolve environmental light Drosophila. This performance is achieved by the smallest rhab- fl patterns (1–3). Typically, compound eyes are roughly spherical in domeres ever reported in a ying insect, which (i) reduce blur shape, sectored into arrays of lens-capped sampling units, named and cross-talk between photoreceptors, improving spatial reso- ommatidia, which accept light from narrow angles (3), de- lution as required for its predatory lifestyle, and (ii) incorporate termining their sampling resolution (4). Although the eye’s sam- microvillar phototransduction reactions with drastically reduced pling resolution can improve when its lenses shrink, their projected processing delays, enabling them to transmit even higher in- image blurs more because of diffraction (5). The optimal lens formation rates than photoreceptors of much larger Calliphora diameter, which is expected when these two limits nearly meet, flies. Furthermore, we report local specializations in the Coe- scales with the square root of the eye size across many insect nosia eye consistent with an acute zone, evidencing that local species (5), implying high resolution as their design objective. specializations of the eye are not confined to larger animals. However, smaller lenses collect less light, reducing the signal-to- noise ratio (SNR) of the sampled image (4). Although the lenses perform light collection, the focal length of the lens and the di- Author contributions: P.T.G.-B., T.J.W., and M.J. designed and performed research; M.J. ameter of the light guides, or rhabdomeres, finally determine the contributed new reagents/analytic tools; P.T.G.-B., T.J.W., and M.J. analyzed data and wrote the paper; P.T.G.-B. and T.J.W. had the idea of using Coenosia and did microscopy/video; pixel size (6). In combination, lens diameter, rhabdomere width, P.T.G.-B. recorded spatial data; and M.J. recorded temporal data. and focal length impose a tradeoff between spatial resolution and The authors declare no conflict of interest. sensitivity (intensity resolution), which is thought to be further This article is a PNAS Direct Submission. S.B. is a guest editor invited by the Editorial aggravated the smaller the eyes (3, 7, 8). Board. Ultimately, because the demands for pattern recognition differ 1Present address: Janelia Farm Research Campus, Howard Hughes Medical Institute, greatly for different visual tasks and habitats (9), the selected eye Ashburn, VA 20147. design should reflect the insect’s lifestyle (3) and the versatility of 2To whom correspondence should be addressed. E-mail: m.juusola@sheffield.ac.uk. neural information processing in its visual system (10). A fast- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. flying aerial predator needs to resolve rapidly changing in- 1073/pnas.1014438108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1014438108 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 Results Visual Performance and Body Size. Our video footage confirmed previous field observations that Coenosia outperform Drosophila in visual flight control; Coenosia catch Drosophila midflight (Movie S1), consuming their prey after landing (Fig. 1 A and B). Coenosia have larger eyes than Drosophila (Fig. 1 C–E). In the case of male Coenosia, whose body size is similar to that of Drosophila, the larger eyes indicate a higher investment in the visual system. Larger eyes can support bigger and/or more sampling units and may provide the eye with a larger sampling area. However, if the sampling area stays constant and other eye parameters (i.e., focal length, rhabdomere width, etc.) are un- changed, larger and thus fewer lenses increase sensitivity by collecting light over a wider angle, at the expense of sampling resolution. The reverse also holds: boasting more but smaller lenses narrows the interommatidial angles, which improves the sampling resolution at the expense of sensitivity. To investigate how the larger eye of Coenosia is used, we counted and measured the lenses and gauged the interommatidial angles across the eyes of both species. Lens Metrics and Interommatidial Angles. We found that Coenosia has two to three times more lenses than Drosophila, but their average sizes are similar (Table S1). Although the Drosophila eye Fig. 2. Lens diameter (D) and interommatidial angle (Δφ) across the eyes shows no obvious regional specializations (lens diameter = 16.85 fi μm ± 0.21 SEM), the lens diameter of Coenosia increases sig- (miniature gures to the right indicate the sectioning plane used for each fi graph). (A) Eyes were divided into anterior, lateral, and posterior regions ni cantly from the posterior toward the front of the eye, yielding and the respective lens diameters measured from several locations for each −5 values between 14 and 20 μm(P < 10 ) for females and between region (n = 1 for each genotype). For each location, the mean distance (n =5) −5 13 and 17 μm(P < 10 ) for males (Fig. 2A). The larger frontal between the center of neighboring lenses is plotted on the x axis, according lenses of Coenosia indicate local specializations for either in- to their estimated horizontal position. (B) Mean interommatidial angles creased sensitivity (bright zone) or resolution (acute zone). from horizontal cuts of ♀ Coenosia and Drosophila. Coenosia have the ’ smallest Δφ in the anterior (frontal) region (Δφ = 1.88°) (n = 2). (C) Even To determine whether Coenosia s frontal lenses sample the Δφ environment at higher spatial frequencies than (i) the remainder when the center of the acute zone is not sectioned (Fig. S2A), mean in Coenosia reach smaller values than Drosophila (n = 2 for each genotype). (Scale bars, 200 μm.) of the Coenosia eye and (ii) Drosophila frontal lenses, we mea- sured the interommatidial angles (Δφ), which describes the cornea sampling density (18). Using semithin horizontal sections from resin-embedded samples, we located the smallest inter- ommatidial angles at the front of the Coenosia eye (Δφ = 2.2° ± 0.08 SEM; Fig.