The role of the ocelli in the phototactic behaviour of the haematophagous bug Triatoma infestans

In addition to compound eyes, most adult insects posses two or three simple eyes, the ocelli. The function of these photoreceptors remains elusive in most cases. Triatomine bugs posses two well-developed ocelli, located in a latero-dorsal position, behind the compound eyes. We tested the role of the ocelli in the phototactic behaviour of Triatoma infestans, by measuring the time spent by adult males in the dark half of an experimental arena, which had the other half illuminated. The occlusion of the ocelli or the compound eyes alone had little effect on the phototactic response of the bugs. Only those insects which had both their ocelli and compound eyes occluded showed a significant reduction in their negative response to light. The ability of the ocelli of T. infestans to mediate the phototactic response by themselves (i.e., not through the modulation of compound eyes sensitivity) constitutes the first report on this function in insects.     

昆虫单眼的结构和功能

大多数昆虫的视觉器官除了复眼外还有一些简单的小眼,称为单眼。昆虫成虫和半变态类若虫的单眼称为背单眼,位于头顶两复眼之间。背单眼在数目和结构上都有较大变化,但基本结构包括角膜晶体、一层角膜生成细胞(覆盖在角膜晶体上)、视网膜(由大约1000个感光细胞构成,视类群而不同)。背单眼对弱光比较敏感,但在图像感知方面的作用并不显著;它是一种“激发器官”,可以增加复眼的感知能力。全变态昆虫的幼虫既没有复眼也没有背单眼,但在其头部两侧有些类似复眼小眼的侧单眼。侧单眼的结构也与小眼相似,包括角膜,晶体和由一些视网膜细胞组成的视杆。侧单眼是完全变态类昆虫幼虫仅有的感光器官,与复眼一样,它们可以感知颜色、形状、距离等等。     

Distribution of photoperiodic receptors in the compound eyes of the bean bug, Riptortus clavatus

  The bean bug, Riptortus clavatus shows a long-day photoperiodic response with respect to the control of adult diapause. The location of photoreceptors for photoperiodism was examined in this species by complete or partial removal of photoreceptor organs. Even after one compound eye or both ocelli were removed, the insects were sensitive to photoperiod. After both compound eyes were removed, however, the insects became reproductive regardless of the photoperiod. Therefore, photoreceptors for photoperiodism were not in the ocelli but in the compound eyes. To clarify whether ommatidia in compound eyes have a regional difference in reception of photoperiod, sensitivity to photoperiod was examined after one compound eye and a part of the contralateral one were removed. Only when the central region of compound eyes was removed did the insects lose sensitivity to photoperiod. It is concluded that the ommatidia in the central region of compound eyes play a principal role in the reception of photoperiod. Accepted: 23 September 1996     

Homothorax controls a binary Rhodopsin switch in Drosophila ocelli

Visual perception of the environment is mediated by specialized photoreceptor (PR) neurons of the eye. Each PR expresses photosensitive opsins, which are activated by a particular wavelength of light. In most insects, the visual system comprises a pair of compound eyes that are mainly associated with motion, color or polarized light detection, and a triplet of ocelli that are thought to be critical during flight to detect horizon and movements. It is widely believed that the evolutionary diversification of compound eye and ocelli in insects occurred from an ancestral visual organ around 500 million years ago. Concurrently, opsin genes were also duplicated to provide distinct spectral sensitivities to different PRs of compound eye and ocelli. In the fruit fly Drosophila melanogaster, Rhodopsin1 (Rh1) and Rh2 are closely related opsins that originated from the duplication of a single ancestral gene. However, in the visual organs, Rh2 is uniquely expressed in ocelli whereas Rh1 is uniquely expressed in outer PRs of the compound eye. It is currently unknown how this differential expression of Rh1 and Rh2 in the two visual organs is controlled to provide unique spectral sensitivities to ocelli and compound eyes. Here, we show that Homothorax (Hth) is expressed in ocelli and confers proper rhodopsin expression. We find that Hth controls a binary Rhodopsin switch in ocelli to promote Rh2 expression and repress Rh1 expression. Genetic and molecular analysis of rh1 and rh2 supports that Hth acts through their promoters to regulate Rhodopsin expression in the ocelli. Finally, we also show that when ectopically expressed in the retina, hth is sufficient to induce Rh2 expression only at the outer PRs in a cell autonomous manner. We therefore propose that the diversification of rhodpsins in the ocelli and retinal outer PRs occurred by duplication of an ancestral gene, which is under the control of Homothorax.     

蝗虫复眼光谱敏感性的比较研究——Ⅱ.视网膜电图的光谱敏感曲线

(1)用视网膜电图(ERG)方法测定了9种蝗虫在黑暗、蓝光和橙光适应下的光谱敏感性。(2)9种蝗虫的碚适应光谱敏感曲线峰值均在520—546nm 之间。(3)橙光或蓝光明适应导致不同程度的峰值位移,蓝区的相对敏感性提高,这与光引起屏蔽色素移动效应有关。(4)黑背蝗和稻蝗复眼表面均没有黑白间,橙光适应时出现第二个峰值在蓝区,而蓝光适应则压抑蓝区的敏感性。可能这两种蝗虫还具有蓝敏视色素。(5)佛蝗和黄脊蝗复眼表面均有明显的黑白相间的区域,在有色光适应下这两种蝗虫的光谱敏感性变化最小,没有证据说明多于一种光敏色素。     

Opsin evolution and expression in Arthropod compound Eyes and Ocelli: Insights from the cricket Gryllus bimaculatus

ABSTRACT: BACKGROUND: Opsins are key proteins in animal photoreception. Together with a light-sensitive group, the chromophore, they form visual pigments which initiate the visual transduction cascade when photoactivated. The spectral absorption properties of visual pigments are mainly determined by their opsins, and thus opsins are crucial to understand the adaptations of animal eyes. Studies on the phylogeny and expression pattern of opsins have received considerable attention, but our knowledge about insect visual opsins is still limited. Up to now, researchers have focused on holometabolous insects, while general conclusions require sampling from a broader range of taxa. We have therefore investigated visual opsins in the ocelli and compound eyes of the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect. RESULTS: Phylogenetic analyses place all identified cricket sequences within the three main visual opsin clades of insects. We assign three of these opsins to visual pigments found in the compound eyes with peak absorbances in the green (515 nm), blue (445 nm) and UV (332 nm) spectral range. Their expression pattern divides the retina into distinct regions: (1) the polarization-sensitive dorsal rim area with blue- and UV-opsin, (2) a newly-discovered ventral band of ommatidia with blue- and green-opsin and (3) the remainder of the compound eye with UV- and green-opsin. In addition, we provide evidence for two ocellar photopigments with peak absorbances in the green (511 nm) and UV (350 nm) spectral range, and with opsins that differ from those expressed in the compound eyes. CONCLUSIONS: Our data show that cricket eyes are spectrally more specialized than has previously been assumed, suggesting that similar adaptations in other insect species might have been overlooked. The arrangement of spectral receptor types within some ommatidia of the cricket compound eyes differs from the generally accepted pattern found in holometabolous insect taxa and awaits a functional explanation. From the opsin phylogeny, we conclude that gene duplications, which permitted differential opsin expression in insect ocelli and compound eyes, occurred independently in several insect lineages and are recent compared to the origin of the eyes themselves.     

The Spectral Sensitivities of Single Receptor Cells in the Lateral, Median, and Ventral Eyes of Normal and White-Eyed Limulus

Spectral sensitivity curves can be distorted by screening pigments. We have determined whether this is true for Limulus polyphemus by determining, from receptor potentials recorded using intracellular microelectrodes, spectral sensitivity curves for normal animals and for white-eyed animals (which lack screening pigment). Our results show: (a) In median ocelli, the curve for UV-sensitive receptor cells peaks at 360 nm and does not depend on the presence of screening pigment, (b) The curve for ventral eye photoreceptors is identical to that for retinular cells from the lateral eyes of white-eyed animals and peaks at 520–525 nm. (c) In normal lateral eyes, when the stimulating light passes through screening pigment, the curve indicates relatively more sensitivity in the red region of the spectrum than does the curve for white-eyed animals. Therefore, the screening pigment is probably red-transmitting, (d) In median ocelli, the curve for visible-sensitive cells peaks at 525 nm and is approximately the same whether the ocelli are from normal or white-eyed animals. However, the curve is significantly broader than that for ventral eyes and for lateral eyes from white-eyed animals.     

Localization of the photoreceptor for photoperiodism in the stink bug, Plautia crossota stali

The brown-winged green bug Plautia crossota stali Scott (Heteroptera: Pentatomidae) shows a long-day photoperiodic response with respect to the control of adult diapause. The location of the photoreceptor for this response was examined by surgical removal of putative photoreceptor organs. Even after both ocelli were removed, the insects responded normally to the photoperiod. After bilateral removal of the compound eyes, the insects developed reproductive organs and the volume of the corpus allatum increased regardless of photoperiod. Therefore, the compound eyes play a major role in the reception of photic information for photoperiodism in P. c. stali. However, because removal of the bilateral compound eyes did not completely prevent the response to photoperiod, photoreceptors other than the compound eyes can also receive photic information for photoperiodism.     

夜行性昆虫微光视觉行为及其视觉适应机制

作为昆虫种群的重要组成部分,夜行性昆虫成功进化出了与其生存环境相适应的感觉机制,普遍认为夜行性昆虫主要依靠嗅觉和机械性感受等来探索环境,其视觉器官发生了退化或功能丧失。近年来,随着红外夜视、视网膜电位(electroretinogram, ERG)和视觉神经等生物新技术的应用,昆虫视觉生态学研究出现了突破性进展,自2002年以来陆续发现蛾类、蜜蜂和蜣螂等夜行性昆虫进化出了非凡的微光视觉(dim-light vision)能力,在夜晚(光照强度低于0.3 lx)依然可以如同在明亮的白天一样清晰、准确地感知目标物体特定的视觉特性,如明暗、颜色、形状、大小、对比度、偏振光和运动状态等,展现出视觉调控夜行性昆虫行为活动的巨大潜力。此外,这些夜行性昆虫复眼瞳孔、小眼焦距、视杆和色素颗粒等方面进化出了一些相应的形态生理特征,以提高光学灵敏度适应夜间微光环境。鉴于夜行性昆虫微光视觉行为及其视觉适应机制的研究尚处于起步阶段,仅见于少数访花昆虫或粪食性昆虫,建议加强以下几个方面的研究：(1)重大夜行性农业害虫的微光视觉及其应用的研究;(2)非典型重叠复眼的光学结构特征及其应对微光环境的适应机制研究;(3)夜行性昆虫响应微光环境的视觉适应机制研究;(4)基于夜行性昆虫微光视觉行为研发新型害虫防控技术。     

Hornets Can Fly at Night without Obvious Adaptations of Eyes and Ocelli

Hornets, the largest social wasps, have a reputation of being facultatively nocturnal. Here we confirm flight activity of hornet workers in dim twilight. We studied the eyes and ocelli of European hornets (Vespa crabro) and common wasps (Vespula vulgaris) with the goal to find the optical and anatomical adaptations that enable them to fly in dim light. Adaptations described for obligately nocturnal hymenoptera such as the bees Xylocopa tranquebarica and Megalopta genalis and the wasp Apoica pallens include large ocelli and compound eyes with wide rhabdoms and large facet lenses. Interestingly, we did not find any such adaptations in hornet eyes or ocelli. On the contrary, their eyes are even less sensitive than those of the obligately diurnal common wasps. Therefore we conclude that hornets, like several facultatively nocturnal bee species such as Apis mellifera adansonii, A. dorsata and X. tenuiscapa are capable of seeing in dim light simply due to the large body and thus eye size. We propose that neural pooling strategies and behavioural adaptations precede anatomical adaptations in the eyes and ocelli when insects with apposition compound eyes turn to dim light activity.     

蟋蟀视觉系统的解剖结构与生理机能

蟋蟀视觉系统由单眼、复眼、视叶三部分组成。蟋蟀的单眼为背单眼,由角膜、角膜生成细胞、视网膜等组成,是提高昆虫复眼所感知的视觉刺激的兴奋水平部位;复眼是最主要的视觉器官,由角膜、晶锥、感杆束和网膜细胞、基膜组成,是光电转导和视觉级联反应的中心;视叶由神经节层、外髓和内髓组成,是视觉神经系统的中心。     

Induction of reproductive diapause via perception of photoperiod through the compound eyes in the adult blow fly, Protophormia terraenovae

Covering and surgical removal of the compound eyes were performed to localize photoreceptors for photoperiodic responses in the blow fly Protophormia terraenovae (Diptera, Calliphoridae). Adult females showed a long-day photoperiodic response to control reproductive diapause. When the compound eyes were bilaterally covered with silver paint, diapause incidence increased under diapause-preventing conditions, i.e., a long-day photoperiod and constant light, as though flies were kept under constant darkness. Neither silver painting on a medial region of the head capsule nor control painting in which both compound eyes were painted in a clear solvent caused significant effects on diapause incidence. Unilateral painting of the compound eye caused an increment of diapause incidence under constant light but no effects under a long-day photoperiod. When the compound eyes were bilaterally removed, all the flies developed their ovaries both under a long-day and a short-day photoperiod. Unilateral removal of the compound eye also caused ovarian development under a short-day photoperiod, whereas removal of one antennal lobe or all ocelli caused no effects on diapause incidence. Since P. terraenovae completely lost responsiveness to photoperiod after blinding of the compound eyes, it is likely that this fly perceives photoperiod through its compound eyes. Accepted: 18 February 1997     

Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles

Most bees are diurnal, with behaviour that is largely visually mediated, but several groups have made evolutionary shifts to nocturnality, despite having apposition compound eyes unsuited to vision in dim light. We compared the anatomy and optics of the apposition eyes and the ocelli of the nocturnal carpenter bee, Xylocopa tranquebarica, with two sympatric species, the strictly diurnal X. leucothorax and the occasionally crepuscular X. tenuiscapa. The ocelli of the nocturnal X. tranquebarica are unusually large (diameter ca. 1 mm) and poorly focussed. Moreover, their apposition eyes show specific visual adaptations for vision in dim light, including large size, large facets and very wide rhabdoms, which together make these eyes 9 times more sensitive than those of X. tenuiscapa and 27 times more sensitive than those of X. leucothorax. These differences in optical sensitivity are surprisingly small considering that X. tranquebarica can fly on moonless nights when background luminance is as low as 10⁻⁵ cd m⁻², implying that this bee must employ additional visual strategies to forage and find its way back to the nest. These strategies may include photoreceptors with longer integration times and higher contrast gains as well as higher neural summation mechanisms for increasing visual reliability in dim light.     

Colour in the eyes of insects

Many insect species have darkly coloured eyes, but distinct colours or patterns are frequently featured. A number of exemplary cases of flies and butterflies are discussed to illustrate our present knowledge of the physical basis of eye colours, their functional background, and the implications for insect colour vision. The screening pigments in the pigment cells commonly determine the eye colour. The red screening pigments of fly eyes and the dorsal eye regions of dragonflies allow stray light to photochemically restore photoconverted visual pigments. A similar role is played by yellow pigment granules inside the photoreceptor cells which function as a light-controlling pupil. Most insect eyes contain black screening pigments which prevent stray light to produce background noise in the photoreceptors. The eyes of tabanid flies are marked by strong metallic colours, due to multilayers in the corneal facet lenses. The corneal multilayers in the gold-green eyes of the deer fly Chrysops relictus reduce the lens transmission in the orange-green, thus narrowing the sensitivity spectrum of photoreceptors having a green absorbing rhodopsin. The tapetum in the eyes of butterflies probably enhances the spectral sensitivity of proximal long-wavelength photoreceptors. Pigment granules lining the rhabdom fine-tune the sensitivity spectra.     

The role of ocelli in circadian singing rhythms of crickets

ABSTRACT. . There is a direct quantitative relationship between the free-running period (r) of the circadian stridulation rhythm of male Australian field crickets, Teleogryllus commodus (Walker), and the intensity of the constant light conditions. Both T. commodus and the house cricket, Acheta domesticus (L.), show free-running periods of the singing rhythm of c. 24 h when the light intensity is 0.00025 lux. In both species the severance of the three ocellar nerves significantly slows the circadian period which is indicative of a reduced perception of the available light intensity. To test whether this period reduction is a peripheral or a central effect, electro-retinograms (ERGs) were recorded from compound eyes of male T. commodus with the ocelli fully functional, then occluded, and then uncovered. The size of the compound eye ERG is reduced by 20% with ocellar occlusion and can subsequently be fully restored to the intact level, which indicates that the ocellar effect is a peripheral one. Intensified CoCl₂ fills reveal one neurone in A. domesticus and two in T. commodus which travel from the lateral ocellar nerve out into the ipsilateral optic lobe of the compound eye. These neurones all terminate in or distal to the lobular neuropile. The data are interpreted to indicate a role for ocelli in modulating the light intensity perception of the compound eye. The final effect of the ocellar afferents is at a peripheral level prior to the input of the visual information to the optic lobe circadian pacemaker. Hence ocelli play an indirect role in circadian rhythmicity, augmenting the sensitivity of the primary photoreceptors to better perceive photic entrainment signals.     

An insect retina without microvilli in the male scale insect,Eriococcus sp. (Eriococcidae,Homoptera)

Summary Male scale insects of an undescribed Australian species of Eriococcus have no compound eyes but show an extraordinary arrangement of three pairs of ocelli: One pair is positioned dorsolaterally where most insects have their compound eyes. Another pair looks ventrally and is placed where insects usually have their mouthparts, and there are two small lateral ocelli. Corneal nipples and a spherical lens with an estimated F-number only 0.55 are structural adaptations considered to increase the overall light sensitivity in order to compensate for the poor quantum capture of the shallow retina whose rhabdomes are only 3 m long. The outer segment of each receptor cell consists of a central core of cytoplasm containing mitochondria and a peripheral cylinder of about 16 rhabdomeres. There is no optical separation between neighbouring outer segments. Uniquely in arthropod eyes, the light sensitive structures are not composed of cylindrical microvilli, but consist of membrane stacks whose configuration is analogous to the stacked plates of vertebrate cones. At present no conclusive answer can be given as to why the photoreceptors have plates instead of microvilli. Comparative calculations show that they do not contain more photosensitive membrane per unit volume than rhabdomeres of fly ocelli.     

Single and Multiple Visual Systems in Arthropods

Extraction of two visual pigments from crayfish eyes prompted an electrophysiological examination of the role of visual pigments in the compound eyes of six arthropods. The intact animals were used; in crayfishes isolated eyestalks also. Thresholds were measured in terms of the absolute or relative numbers of photons per flash at various wavelengths needed to evoke a constant amplitude of electroretinogram, usually 50 µv. Two species of crayfish, as well as the green crab, possess blue- and red-sensitive receptors apparently arranged for color discrimination. In the northern crayfish, Orconectes virilis, the spectral sensitivity of the dark-adapted eye is maximal at about 550 mµ, and on adaptation to bright red or blue lights breaks into two functions with λ_max respectively at about 435 and 565 mµ, apparently emanating from different receptors. The swamp crayfish, Procambarus clarkii, displays a maximum sensitivity when dark-adapted at about 570 mµ, that breaks on color adaptation into blue- and red-sensitive functions with λ_max about 450 and 575 mµ, again involving different receptors. Similarly the green crab, Carcinides maenas, presents a dark-adapted sensitivity maximal at about 510 mµ that divides on color adaptation into sensitivity curves maximal near 425 and 565 mµ. Each of these organisms thus possesses an apparatus adequate for at least two-color vision, resembling that of human green-blinds (deuteranopes). The visual pigments of the red-sensitive systems have been extracted from the crayfish eyes. The horse-shoe crab, Limulus, and the lobster each possesses a single visual system, with λ_max respectively at 520 and 525 mµ. Each of these is invariant with color adaptation. In each case the visual pigment had already been identified in extracts. The spider crab, Libinia emarginata, presents another variation. It possesses two visual systems apparently differentiated, not for color discrimination but for use in dim and bright light, like vertebrate rods and cones. The spectral sensitivity of the dark-adapted eye is maximal at about 490 mµ and on light adaptation, whether to blue, red, or white light, is displaced toward shorter wavelengths in what is essentially a reverse Purkinje shift. In all these animals dark adaptation appears to involve two phases: a rapid, hyperbolic fall of log threshold associated probably with visual pigment regeneration, followed by a slow, almost linear fall of log threshold that may be associated with pigment migration.     

昆虫复眼形态结构及感光机制研究进展

复眼是昆虫的主要视觉器官,昆虫复眼形态、结构的研究是理解昆虫感光的基础。本文从昆虫复眼的外部形态、内部微观结构和功能以及对光的感受机制作一简要综述,且对今后昆虫复眼的研究方向进行了展望。     

A retinal substrate for colour discrimination in crabs

Summary In crabs, there is behavioural evidence for colour discrimination from the portunidCarcinus and severalUca species, but in the same and related species only a single visual pigment has been found in the rhabdoms by microspectrophotometry. Micro-electrode recordings of the spectral sensitivity of single portunid photoreceptors may throw some light on this apparent inconsistency. Large changes in spectral sensitivity occur with light adaptation in the crabScylla serrata. Selective adaptation experiments rule out the possibility that the changes may be caused by the presence of a number of visual pigments or of antenna pigments. The results suggest that inScylla the absorption of a single visual pigment type is modified by different coloured filters in different photoreceptors and that this makes colour discrimination possible.     

The roles ofDrosophila ocelli and compound eyes in phototaxis

Summary Drosophila have three types of photoreceptors in their compound eyes: R1–6, R7, and R8. In addition they have simple eyes, ocelli, with another type of photoreceptor. The role of each type of receptor and the possible interaction of their inputs were examined in an innate visual preference task, fast walking phototaxis. Flies were found to be attracted to light, i.e., positively phototactic. We compared the strength of the photopositive response and the spectral preference of normal fly strains and mutant fly strains lacking functional ocelli, R1–6, or R7, singly or in combination. Electroretinographic measures were used to confirm the specificity of deficits in visual mutant strains and the normal functioning of intact receptors.The strength of the photopositive response was strong, as indicated by the high correlation between increases in the intensity of the variable stimulus and increasing numbers of flies attracted toward it. Nearly all strains with or without intact receptor types showed high correlations whether the constant intensity stimulus offered as the alternative choice was bright 467 nm light (Figs. 1 and 2) or dim 572 nm light (Figs. 3 and 4). These constant stimuli were selected so that data in relevant intensity ranges of receptor function would be obtained. An important exception to the high correlations in the intensityresponse functions occurred with flies lacking function in all receptor types except R8; their positive phototaxis was extremely weak in dim light (Fig. 3).Analyses of the phototactic spectral sensitivities (Figs. 5 and 6), as well as comparisons with known electrophysiological spectral sensitivities, were used to determine the inputs from compound eye receptors and to demonstrate central interaction of these inputs with ocellar input. Several experiments with converging evidence suggest that R7 (when present) and R8 dominate fast phototaxis in the conditions of our experiment. R1–6 is the predominant compound eye receptor type in ERG measures; however, its behavioral input is clearly demonstrated only as enhancing R8 dominance of phototaxis in experiments using a dim constant stimulus and as enhancing R7 dominance of phototaxis in experiments using a bright constant stimulus. Similarly, the presence of ocellar receptors also facilitates R8 input in dim light and R7 input in bright light. The data substantiating these respective conclusions are: (1) a lack of dim light phototaxis in a mutant strain with only R8 functional (Fig. 3); and (2) a lack of an ultraviolet (UV) maximum from R7 in bright light phototaxis in a mutant strain with only R7 and R8 functional (Fig. 5c).Generally, absence of the ocelli and R1–6 had remarkably little effect on fast phototactic behavior except for the interaction with R7 and R8 inputs. This interaction is consistent with a theory that ocelli serve to modulate compound eye sensitivity.Abbreviations ERG electroretinogram - PDA prolonged depolarizing afterpotential - R (1–6, 7, 8) retinular cell(s) - UV ultraviolet We thank K. Frayer, F. Garfinkel, K. Hansen, M. Johnson, R. Srygley, and G. Sullivan for technical assistance; K. Hansen was instrumental in running the experiments at extremely dim conditions. Supported by grants NSF-BNS-76-11921 and NIH-1-RO1-EY-02487-01A1 (to W.S.S.). Experiments reported in this paper were included in a dissertation (Karin G. Hu) submitted in partial fulfillment of the requirements of the Ph.D. degree to the Department of Psychology, The Johns Hopkins University, Baltimore, Maryland 21218. We thank members of the Graduate Board Dissertation Examining Committee for their comments: Drs. E. Blass, R. DeVoe, K. Muller and W. Sofer.