High-speed imaging of light-induced photoreceptor microsaccades in compound eyes

Inside compound eyes, photoreceptors contract to light changes, sharpening retinal images of the moving world in time. Current methods to measure these so-called photoreceptor microsaccades in living insects are spatially limited and technically challenging. Here, we present goniometric high-speed deep pseudopupil (GHS-DPP) microscopy to assess how the rhabdomeric insect photoreceptors and their microsaccades are organised across the compound eyes. This method enables non-invasive rhabdomere orientation mapping, whilst their microsaccades can be locally light-activated, revealing the eyes' underlying active sampling motifs. By comparing the microsaccades in wild-type Drosophila's open rhabdom eyes4 to spam-mutant eyes, reverted to an ancestral fused rhabdom state, we show how two different eye types sample light information. These results show different ways how vision converts space into time, and highlight how compound eyes and their active sampling can evolve with insects' visual needs.

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

The common backswimmer, Notonecta glauca , uses vision by day and night for functions such as underwater prey animal capture and flight in search of new habitats. Although previous studies have identified some of the physiological mechanisms facilitating such flexibility in the animal's vision, neither the biophysics of Notonecta photoreceptors nor possible cellular adaptations are known. Here, we studied Notonecta photoreceptors using patch-clamp and intracellular recording methods. Photoreceptor size (approximated by capacitance) was positively correlated with absolute sensitivity and acceptance angles. Information rate measurements indicated that large and more sensitive photoreceptors performed better than small ones. Our results suggest that backswimmers are adapted for vision in both dim and well-illuminated environments by having open-rhabdom eyes with large intrinsic variation in absolute sensitivity among photoreceptors, exceeding those found in purely diurnal or nocturnal species. Both electrophysiology and microscopic analysis of retinal structure suggest two retinal subsystems: the largest peripheral photoreceptors provide vision in dim light and the smaller peripheral and central photoreceptors function primarily in sunlight, with light-dependent pigment screening further contributing to adaptation in this system by dynamically recruiting photoreceptors with varying sensitivity into the operational pool.

An exceptionally well-preserved Eocene dolichopodid fly eye: function and evolutionary significance

The exceptionally preserved eyes of an Eocene dolichopodid fly contained in Baltic amber show remarkable detail, including features at micrometre and submicrometre levels. Based on this material, we establish that it is likely that the neural superposition compound eye existed as far back as 45 Ma. The ommatidia have an open rhabdom with a trapezoidal arrangement of seven rhabdomeres. Such a structure is uniquely characteristic of the neural superposition compound eye of present-day flies. Optical analysis reveals that the fossil eyes had a sophisticated and efficient optical system.

Light-induced and circadian changes in the compound eye of the haematophagous bug Triatoma infestans (Hemiptera: Reduviidae)

SUMMARY We analysed dynamic changes in the ommatidial structure of the compound eyes of Triatoma infestans. This nocturnal insect possesses open-rhabdom eyes, in which a ring of six rhabdomeres from retinula cells 1–6 (R1–6) surrounds a central pair of rhabdomeres from retinula cells 7 and 8 (R7–8). Screening pigments are located in all the photoreceptors and in the primary (PPC) and secondary (SPC) pigment cells. During the day, pigments within R1–6 and the PPCs form a small ‘pupil’ above the rhabdom and pigments within R7–8 are clustered around the central rhabdomere, allowing light to reach only the central rhabdomere. At night, the ‘pupil’ widens, and pigments inside R7–8 concentrate in the proximal region of the cells, allowing light to reach the peripheral rhabdomeres. In addition, the distance between the cornea and the rhabdom decreases. These rhythmic changes adapt the sensitivity of the eye by controlling the amount of light reaching and travelling within the rhabdom. Furthermore, the rhythm persists under conditions of constant darkness (DD), i.e. it is controlled by an endogenous oscillator. Remarkably, there are differences in pigment movements between the retinula cells of a single ommatidium. The migration of pigments in R1–6 is regulated by a circadian input, while that in R7–8 is regulated by both direct light and circadian inputs. The rhythm vanishes under constant-light conditions (LL). In this species, the circadian rhythm of photonegative behaviour persists in both DD and LL conditions, suggesting that these two rhythms, in retinal morphology and visual behaviour, may be generated by different circadian oscillators.

Fine structure of the compound eye of the black fly Simulium vittatum (Diptera: Simuliidae)

The fine structure of the ommatidia in light- and dark-adapted eyes of male and female Simulium vittatum Zetterstedt was investigated using scanning and transmission electron microscopy. The male eye is divided into distinct dorsal and ventral regions. The facets in the dorsal region are approximately two times larger than those in the ventral one, which are similar in size to the ones in the female eye. All ommatidia of S. vittatum examined consist of two general regions: a distal dioptric apparatus with bordering primary and accessory pigment and Semper cells, and a sensory receptor layer. Each ommatidium in the female eye and ventral eye of the male has eight retinular cells (R cells): six peripheral (R1–6) and two central (R7, R8). R7 occurs distally and R8 basally. Strikingly, the ommatidia in the dorsal eye of the male lack the R7 cell. In all ommatidia, rhabdomeres on the inner surface of the peripheral R cells are separate throughout their length, creating an open rhabdom. A greater diameter of corneal facets, elongated peripheral R cells, and perhaps the lack of the R7 cell are specializations of the dorsal region of the eye that help the male to detect small, rapidly moving females against the skylight as they fly above the swarm of males. Differences observed between light- and dark-adapted eyes of male and female S. vittatum were the same and were associated with the internal components of the peripheral R cells.

The phylogenetic significance of ommatidium structure in the compound eyes of polyphagan beetles

The structure of ommatidia in adults of more than 200 beetle species from 91 polyphagan families was surveyed. Three basic types of lens system (eucone, exocone, and acone) and two types of retinal unit (fused rhabdom, open rhabdom) are represented. The eucone (crystalline cone-containing) ommatidium is ancestral and prevails in primitive Eucinetoidea, Hydrophiloidea, and Scarabaeoidea; ommatidia of the primitive beetles Cupes and Omma as well as the Adephaga are of this type. The polyphagan founders most likely had ommatidia with small crystalline cones and narrow clear zones beneath the corneal facets. Exocone and acone eyes are derived structures, and their distribution suggests that both have evolved several times. Exocone ommatidia arose early in polyphagan evolution, possibly first in dascilloid-like founders of elateriform and bostrychiform beetles, where the exocone is commonly found. An exocone eye also evolved separately in the ancestors of several primitive scarabaeoid families; possible steps in this eucone to exocone transition may be seen in the Trogidae. The clear zones of eucone and exocone eyes are not homologous. The acone ommatidium is specialized and arose through a progressive loss of either crystalline cone or exocone. In the advanced staphylinoid beetles it is a relic of crystalline cone loss in their small ancestors. In the cucujiforms it arose likely from the loss of the exocone in their bostrychiform ancestors, associated here with a shift to an open rhabdom. Although the distribution of ommatidial types coincides with major lineages in the Polyphaga, a few anomalies remain. The Eucnemidae, Buprestidae, and Dryopidae are all eucone yet are placed in the elateriform series, in which 25 of 30 families are exocone. Scarab beetles have an extraordinary variety of lens types that presumably reflects the exceptional adaptability of the eye in this superfamily.