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Background The compound eyes of insects exhibit extensive variation in ommatidia number and size, which affects how they see and underlies adaptations in their vision to different environments and lifestyles. However, very little is known about the genetic and developmental bases of differences in eye size. We previously showed that the larger eyes of Drosophila mauritiana compared to D. simulans are generally caused by differences in ommatidia size rather than number. Furthermore, we identified an X-linked chromosomal region in D. mauritiana that results in larger eyes when introgressed into D. simulans . Results Here, we used a combination of fine-scale mapping and gene expression analysis to further investigate positional candidate genes on the X chromosome. We found earlier expression of orthodenticle (otd) during ommatidial maturation in D. mauritiana than in D. simulans , and we show that this gene is required for the correct organisation and size of ommatidia in D. melanogaster . We discovered that the activity of an otd eye enhancer is consistent with the difference in the expression of this gene between species, with the D. mauritiana enhancer sequence driving earlier expression than that of D. simulans . When otd expression is driven prematurely during D. melanogaster eye development, the ommatidia grow larger, supporting a possible role for the timing of otd expression in regulating ommatidial size. We also identified potential direct targets of Otd that are differentially expressed between D. mauritiana and D. simulans during ommatidial maturation. Conclusions Taken together, our results suggest that differential timing of otd expression may contribute to natural variation in ommatidia size between D. mauritiana and D. simulans , which provides new insights into the mechanisms underlying the regulation and evolution of compound eye size in insects.

This work is a synthesis of our current understanding of the mechanics, aerodynamics and visually mediated control of dragonfly and damselfly flight, with the addition of new experimental and computational data in several key areas. These are: the diversity of dragonfly wing morphologies, the aerodynamics of gliding flight, force generation in flapping flight, aerodynamic efficiency, comparative flight performance and pursuit strategies during predatory and territorial flights. New data are set in context by brief reviews covering anatomy at several scales, insect aerodynamics, neuromechanics and behaviour. We achieve a new perspective by means of a diverse range of techniques, including laser-line mapping of wing topographies, computational fluid dynamics simulations of finely detailed wing geometries, quantitative imaging using particle image velocimetry of on-wing and wake flow patterns, classical aerodynamic theory, photography in the field, infrared motion capture and multi-camera optical tracking of free flight trajectories in laboratory environments. Our comprehensive approach enables a novel synthesis of datasets and subfields that integrates many aspects of flight from the neurobiology of the compound eye, through the aeromechanical interface with the surrounding fluid, to flight performance under cruising and higher-energy behavioural modes. This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.

We describe the development and application of methods for high-throughput neuroanatomy in Drosophila using light microscopy. These tools enable efficient multicolor stochastic labeling of neurons at both low and high densities. Expression of multiple membrane-targeted and distinct epitope-tagged proteins is controlled both by a transcriptional driver and by stochastic, recombinase-mediated excision of transcription-terminating cassettes. This MultiColor FlpOut (MCFO) approach can be used to reveal cell shapes and relative cell positions and to track the progeny of precursor cells through development. Using two different recombinases, the number of cells labeled and the number of color combinations observed in those cells can be controlled separately. We demonstrate the utility of MCFO in a detailed study of diversity and variability of Distal medulla (Dm) neurons, multicolumnar local interneurons in the adult visual system. Similar to many brain regions, the medulla has a repetitive columnar structure that supports parallel information processing together with orthogonal layers of cell processes that enable communication between columns. We find that, within a medulla layer, processes of the cells of a given Dm neuron type form distinct patterns that reflect both the morphology of individual cells and the relative positions of their arbors. These stereotyped cell arrangements differ between cell types and can even differ for the processes of the same cell type in different medulla layers. This unexpected diversity of coverage patterns provides multiple independent ways of integrating visual information across the retinotopic columns and implies the existence of multiple developmental mechanisms that generate these distinct patterns. Significance Nervous systems contain vast numbers of neurons with diverse shapes and complex spatial relationships. We describe new genetic tools for the efficient visualization by light microscopy of individual neurons and their relative positions in Drosophila . The application of these methods to the visual system revealed an unexpected diversity of cell-type–specific arrangements of neuronal processes within a single brain region. This wide range of stereotyped cell arrangements provides distinct circuit elements for processing visual information and implies the existence of a surprisingly large number of genetic programs that produce these arrangements during development.

The ventral compound eye of many insects contains polarization-sensitive photoreceptors, but little is known about how they are integrated into visual functions. In female horseflies, polarized reflections from animal fur are a key stimulus for host detection. To understand how polarization vision is mediated by the ventral compound eye, we investigated the band-eyed brown horsefly Tabanus bromius using anatomical, physiological, and behavioral approaches. Serial electron microscopic sectioning of the retina and single-cell recordings were used to determine the spectral and polarization sensitivity (PS) of photoreceptors. We found 2 stochastically distributed subtypes of ommatidia, analogous to pale and yellow of other flies. Importantly, the pale analog contains an orthogonal analyzer receptor pair with high PS, formed by an ultraviolet (UV)-sensitive R7 and a UV- and blue-sensitive R8, while the UV-sensitive R7 and green-sensitive R8 in the yellow analog always have low PS. We tested horsefly polarotaxis in the field, using lures with controlled spectral and polarization composition. Polarized reflections without UV and blue components rendered the lures unattractive, while reflections without the green component increased their attractiveness. This is consistent with polarotaxis being guided by a differential signal from polarization analyzers in the pale analogs, and with an inhibitory role of the yellow analogs. Our results reveal how stochastically distributed sensory units with modality-specific division of labor serve as separate and opposing input channels for visual guidance.

Until now, the fossil record has not been capable of revealing any details of the mechanisms of complex vision at the beginning of metazoan evolution. Here, we describe functional units, at a cellular level, of a compound eye from the base of the Cambrian, more than half a billion years old. Remains of early Cambrian arthropods showed the external lattices of enormous compound eyes, but not the internal structures or anything about how those compound eyes may have functioned. In a phosphatized trilobite eye from the lower Cambrian of the Baltic, we found lithified remnants of cellular systems, typical of a modern focal apposition eye, similar to those of a bee or dragonfly. This shows that sophisticated eyes already existed at the beginning of the fossil record of higher organisms, while the differences between the ancient system and the internal structures of a modern apposition compound eye open important insights into the evolution of vision.

In most animal species, vision is mediated by compound eyes, which offer lower resolution than vertebrate single-lens eyes, but significantly larger fields of view with negligible distortion and spherical aberration, as well as high temporal resolution in a tiny package. Compound eyes are ideally suited for fast panoramic motion perception. Engineering a miniature artificial compound eye is challenging because it requires accurate alignment of photoreceptive and optical components on a curved surface. Here, we describe a unique design method for biomimetic compound eyes featuring a panoramic, undistorted field of view in a very thin package. The design consists of three planar layers of separately produced arrays, namely, a microlens array, a neuromorphic photodetector array, and a flexible printed circuit board that are stacked, cut, and curved to produce a mechanically flexible imager. Following this method, we have prototyped and characterized an artificial compound eye bearing a hemispherical field of view with embedded and programmable low-power signal processing, high temporal resolution, and local adaptation to illumination. The prototyped artificial compound eye possesses several characteristics similar to the eye of the fruit fly Drosophila and other arthropod species. This design method opens up additional vistas for a broad range of applications in which wide field motion detection is at a premium, such as collision-free navigation of terrestrial and aerospace vehicles, and for the experimental testing of insect vision theories.

The structure of compound eyes in arthropods has been the subject of many studies, revealing important biological principles. Until recently, these studies were constrained by the two-dimensional nature of available ultrastructural data. By taking advantage of the novel three-dimensional ultrastructural dataset obtained using volume electron microscopy, we present the first cellular-level reconstruction of the whole compound eye of an insect, the miniaturized parasitoid wasp Megaphragma viggianii . The compound eye of the female M. viggianii consists of 29 ommatidia and contains 478 cells. Despite the almost anucleate brain, all cells of the compound eye contain nuclei. As in larger insects, the dorsal rim area of the eye in M. viggianii contains ommatidia that are believed to be specialized in polarized light detection as reflected in their corneal and retinal morphology. We report the presence of three ‘ectopic’ photoreceptors. Our results offer new insights into the miniaturization of compound eyes and scaling of sensory organs in general.

Compound eyes formation in decapod crustaceans occurs after the nauplius stage. However, the key genes and regulatory mechanisms of compound eye development during crustacean embryonic development have not yet been clarified. In this study, RNA-seq was used to investigate the gene expression profiles of Neocaridina denticulata sinensis from nauplius to zoea stage. Based on RNA-seq data analysis, the phototransduction and insect hormone biosynthesis pathways were enriched, and molting-related neuropeptides were highly expressed. There was strong cell proliferation in the embryo prior to compound eye development. The formation of the visual system and the hormonal regulation of hatching were the dominant biological events during compound eye development. The functional analysis of DEGs across all four developmental stages showed that cuticle formation, muscle growth and the establishment of immune system occurred from nauplius to zoea stage. Key genes related to eye development were discovered, including those involved in the determination and differentiation of the eye field, eye-color formation, and visual signal transduction. In conclusion, the results increase the understanding of the molecular mechanism of eye formation in crustacean embryonic stage.

Nocturnal insects have evolved remarkable visual capacities, despite small eyes and tiny brains. They can see colour, control flight and land, react to faint movements in their environment, navigate using dim celestial cues and find their way home after a long and tortuous foraging trip using learned visual landmarks. These impressive visual abilities occur at light levels when only a trickle of photons are being absorbed by each photoreceptor, begging the question of how the visual system nonetheless generates the reliable signals needed to steer behaviour. In this review, I attempt to provide an answer to this question. Part of the answer lies in their compound eyes, which maximize light capture. Part lies in the slow responses and high gains of their photoreceptors, which improve the reliability of visual signals. And a very large part lies in the spatial and temporal summation of these signals in the optic lobe, a strategy that substantially enhances contrast sensitivity in dim light and allows nocturnal insects to see a brighter world, albeit a slower and coarser one. What is abundantly clear, however, is that during their evolution insects have overcome several serious potential visual limitations, endowing them with truly extraordinary night vision. This article is part of the themed issue ‘Vision in dim light’.

The visual ecology of flies is outstanding among insects due to a combination of specific attributes. Flies’ compound eyes possess an open rhabdom and thus separate rhabdomeres in each ommatidium assigned to two visual pathways. The highly sensitive, monovariant neural superposition system is based on the excitation of the peripheral rhabdomeres of the retinula cells R1–6 and controls optomotor reactions. The two forms of central rhabdomeres of R7/8 retinula cells in each ommatidium build up a system with four photoreceptors sensitive in different wavelength ranges and thought to account for colour vision. Evidence from wavelength discrimination tests suggests that all colour stimuli are assigned to one of just four colour categories, but cooperation of the two pathways is also evident. Flies use colour cues for various behavioural reactions such as flower visitation, proboscis extension, host finding, and egg deposition. Direct evidence for colour vision, the ability to discriminate colours according to spectral shape but independent of intensity, has been demonstrated for few fly species only. Indirect evidence for colour vision provided from electrophysiological recordings of the spectral sensitivity of photoreceptors and opsin genes indicates similar requisites in various flies; the flies’ responses to coloured targets, however, are much more diverse.