High-resolution vision in pelagic polychaetes.

High-resolution object vision - the ability to separate, classify, and interact with specific objects in the environment against the visual background - has only been conclusively shown to have evolved in three of the thirty-five animal phyla: chordates, arthropods, and mollusks (cephalopods)1. However, alciopid polychaetes (Phyllodocidae, Alciopini), which possess a pair of bulbous camera-type eyes, have also been hypothesized to achieve high acuity. In this study, we examined three species of night-active pelagic alciopids from the Mediterranean Sea. Our optical, morphological, and electrophysiological investigations show that their eyes have high spatial acuity and temporal resolution, supporting the notion that they are capable of active, high-resolution object vision. These results encourage interesting hypotheses about the visual ecology of these enigmatic polychaetes.

Rapid manoeuvre of fan worms (Annelida: Sabellidae) through tubes.

Multiple variables determine the success of an escape response of an animal, and the rapidity of the escape manoeuvre is often the most important. Fan worms (Annelida: Sabellidae) can rapidly withdraw their tentacles, which are covered in heavily ciliated ramifications called pinnules, into their tubes to protect them from approaching threats. Here, we explore the dynamic and mechanistic features behind this escape manoeuvre. The escape responses of fan worms were recorded by high-speed videography and quantified by computerized motion analysis, showing an ultrahigh retraction speed of 272±135 mm s-1 (8±4 body lengths s-1). We found that fan worms possess powerful muscle-driven systems, which can generate contractive forces up to 36 times their body weight. In order to achieve these rapid, forceful movements through seawater without damaging their tentacles, fan worms have developed functional morphological adaptations to reduce fluidic drag, including the flattening of their radiolar pinnules and the deformation of bodily segmental ridges. Our hydrodynamic models indicate that these mechanical processes can decrease fluidic drag by 47%, trapped mass by 75% and friction coefficient by 89%. These strategies allow fan worms to execute rapid escape responses and could inspire the design of fast in-pipe robots.

Colour vision in stomatopod crustaceans.

The stomatopod crustaceans, or mantis shrimps, are colourful marine invertebrate predators. Their unusual compound eyes have dorsal and ventral regions resembling typical crustacean apposition designs separated by a unique region called the midband that consists of from two to six parallel rows of ommatidia. In species with six-row midbands, the dorsal four rows are themselves uniquely specialized for colour analysis. Rhabdoms of ommatidia in these rows are longitudinally divided into three distinct regions: an apical ultraviolet (UV) receptor, a shorter-wavelength middle tier receptor and a longer-wavelength proximal tier receptor. Each of the total of 12 photoreceptors has a different spectral sensitivity, potentially contributing to a colour-vision system with 12 channels. Mantis shrimps can discriminate both human-visible and UV colours, but with limited precision compared to other colour-vision systems. Here, we review the structure and function of stomatopod colour vision, examining the types of receptors present in a species, the spectral tuning of photoreceptors both within and across species, the neural analysis of colour and the genetics underlying the multiple visual pigments used for colour vision. Even today, after many decades of research into the colour vision of stomatopods, much of its operation and its use in nature remain a mystery. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Colour vision in thrips (Thysanoptera).

Insects are an astonishingly successful and diverse group, occupying the gamut of habitats and lifestyle niches. They represent the vast majority of described species and total terrestrial animal biomass on the planet. Their success is in part owed to their sophisticated visual systems, including colour vision, which drive a variety of complex behaviours. However, the majority of research on insect vision has focused on only a few model organisms including flies, honeybees and butterflies. Especially understudied are phytophagous insects, such as diminutive thrips (Thysanoptera), in spite of their damage to agriculture. Thrips display robust yet variable colour-specific responses despite their miniaturized eyes, but little is known about the physiological and ecological basis of their visual systems. Here, we review the known visual behavioural information about thrips and the few physiological studies regarding their eyes. Eye structure, spectral sensitivity, opsin genes and the presence of putative colour filters in certain ommatidia strongly imply dynamic visual capabilities. Finally, we discuss the major gaps in knowledge that remain for a better understanding of the visual system of thrips and why bridging these gaps is important for expanding new possibilities for applied pest management strategies for these tiny insects. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

The Gluopsins: Opsins without the Retinal Binding Lysine.

Opsins allow us to see. They are G-protein-coupled receptors and bind as ligand retinal, which is bound covalently to a lysine in the seventh transmembrane domain. This makes opsins light-sensitive. The lysine is so conserved that it is used to define a sequence as an opsin and thus phylogenetic opsin reconstructions discard any sequence without it. However, recently, opsins were found that function not only as photoreceptors but also as chemoreceptors. For chemoreception, the lysine is not needed. Therefore, we wondered: Do opsins exists that have lost this lysine during evolution? To find such opsins, we built an automatic pipeline for reconstructing a large-scale opsin phylogeny. The pipeline compiles and aligns sequences from public sources, reconstructs the phylogeny, prunes rogue sequences, and visualizes the resulting tree. Our final opsin phylogeny is the largest to date with 4956 opsins. Among them is a clade of 33 opsins that have the lysine replaced by glutamic acid. Thus, we call them gluopsins. The gluopsins are mainly dragonfly and butterfly opsins, closely related to the RGR-opsins and the retinochromes. Like those, they have a derived NPxxY motif. However, what their particular function is, remains to be seen.

Pupil dilation and constriction in the skate Leucoraja erinacea in a simulated natural light field.

The skate Leucoraja erinacea has an elaborately shaped pupil, whose characteristics and functions have received little attention. The goal of our study was to investigate the pupil response in relation to natural ambient light intensities. First, we took a recently developed sensory-ecological approach, which gave us a tool for creating a controlled light environment for behavioural work: during a field survey, we collected a series of calibrated natural habitat images from the perspective of the skates' eyes. From these images, we derived a vertical illumination profile using custom-written software for quantification of the environmental light field (ELF). After collecting and analysing these natural light field data, we created an illumination set-up in the laboratory, which closely simulated the natural vertical light gradient that skates experience in the wild and tested the light responsiveness - in particular the extent of dilation - of the skate pupil to controlled changes in this simulated light field. Additionally, we measured pupillary dilation and constriction speeds. Our results confirm that the skate pupil changes from nearly circular under low light to a series of small triangular apertures under bright light. A linear regression analysis showed a trend towards smaller skates having a smaller dynamic range of pupil area (dilation versus constriction ratio around 4-fold), and larger skates showing larger ranges (around 10- to 20-fold). Dilation took longer than constriction (between 30 and 45 min for dilation; less than 20 min for constriction), and there was considerable individual variation in dilation/constriction time. We discuss our findings in terms of the visual ecology of L. erinacea and consider the importance of accurately simulating natural light fields in the laboratory.

Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas.

Stomatopod crustaceans possess some of the most complex animal visual systems, including at least 16 spectrally distinct types of photoreceptive units (e.g., assemblages of photoreceptor cells). Here we fully characterize the set of opsin genes expressed in retinal tissues and determine expression patterns of each in the stomatopod Neogonodactylus oerstedii Using a combination of transcriptome and RACE sequencing, we identified 33 opsin transcripts expressed in each N. oerstedii eye, which are predicted to form 20 long-wavelength-sensitive, 10 middle-wavelength-sensitive, and three UV-sensitive visual pigments. Observed expression patterns of these 33 transcripts were highly unusual in five respects: 1) All long-wavelength and short/middle-wavelength photoreceptive units expressed multiple opsins, while UV photoreceptor cells expressed single opsins; 2) most of the long-wavelength photoreceptive units expressed at least one middle-wavelength-sensitive opsin transcript; 3) the photoreceptors involved in spatial, motion, and polarization vision expressed more transcripts than those involved in color vision; 4) there is a unique opsin transcript that is expressed in all eight of the photoreceptive units devoted to color vision; and 5) expression patterns in the peripheral hemispheres of the eyes suggest visual specializations not previously recognized in stomatopods. Elucidating the expression patterns of all opsin transcripts expressed in the N. oerstedii retina reveals the potential for previously undocumented functional diversity in the already complex stomatopod eye and is a first step toward understanding the functional significance of the unusual abundance of opsins found in many arthropod species' visual systems.

Differences in signal contrast and camouflage among different colour variations of a stomatopod crustacean, Neogonodactylus oerstedii.

Animal colouration is often a trade-off between background matching for camouflage from predators, and conspicuousness for communication with con- or heterospecifics. Stomatopods are marine crustaceans known to use colour signals during courtship and contests, while their overall body colouration may provide camouflage. However, we have little understanding of how stomatopods perceive these signals in their environment or whether overall body coloration does provide camouflage from predators. Neogonodactylus oerstedii assess meral spot colour during contests, and meral spot colour varies depending on local habitat. By calculating quantum catch for N. oerstedii's 12 photoreceptors associated with chromatic vision, we found that variation in meral spot total reflectance does not function to increase signal contrast in the local habitat. Neogonodactylus oerstedii also show between-habitat variation in dorsal body colouration. We used visual models to predict a trichromatic fish predator's perception of these colour variations. Our results suggest that sandy and green stomatopods are camouflaged from a typical fish predator in rubble fields and seagrass beds, respectively. To our knowledge, this is the first study to investigate signal contrast and camouflage in a stomatopod. These results provide new insight into the function and evolution of colouration in a species with a complex visual system.

Photoresponses in the radiolar eyes of the fan worm Acromegalomma vesiculosum.

Fan worms (Annelida: Sabellidae) possess compound eyes and other photoreceptors on their radiolar feeding tentacles. These eyes putatively serve as an alarm system that alerts the worm to encroaching threats, eliciting a rapid defensive retraction into their protective tube. The structure and independent evolutionary derivation of these radiolar eyes make them a fascinating target for exploring the emergence of new sensory systems and visually guided behaviours. However, little is known about their physiology and how this impacts their function. Here, we present electroretinogram recordings from the radiolar eyes of the fan worm Acromegalomma vesiculosum We examine their spectral sensitivity along with their dynamic range and temporal resolution. Our results show that they possess one class of photoreceptors with a single visual pigment peaking in the blue-green part of the spectrum around 510 nm, which matches the dominant wavelengths in their shallow coastal habitats. We found the eyes to have a rather high temporal resolution with a critical flicker fusion frequency around 35 Hz. The high temporal resolution of this response is ideally suited for detecting rapidly moving predators but also necessitates downstream signal processing to filter out caustic wave flicker. This study provides a fundamental understanding of how these eyes function. Furthermore, these findings emphasise a set of dynamic physiological principles that are well suited for governing a multi-eyed startle response in coastal aquatic habitats.

Developmental studies provide new insights into the evolution of sense organs in Sabellariidae (Annelida).

BACKGROUND: Sabellarids, also known as honeycomb or sandcastle worms, when building their tubes, produce chemical signals (free fatty acids) that are responsible for larval settlement and the formation of three-dimensional aggregations. The larval palps and the dorsal hump (becoming the median organ in adults) are presumed to participate in such a substrate selection during settlement. Notably, the sabellariid median organ is an apparently unique organ among annelids that has been attributed with a sensory function and perhaps with some affinities to the nuchal organs of other polychaetes. Nevertheless, detailed investigations of this prominent character complex including ultrastructural examinations are lacking so far. RESULTS: Our comprehensive investigations provide data about the anterior sensory organs in Sabellariidae and inform about their transformation during pelagic larval development. We used a comparative approach including immunostaining with subsequent confocal laser scanning microscopy (clsm), histological sections as well as electron microscopy in a range of larval and adult stages of two sabellariid species. We find that the neuronal innervation as well as the ultrastructure of the sabellariid ciliary structures along the median organ are highly comparable with that of nuchal organs known from other polychaetes. Furthermore, the myoinhibitory protein (MIP) - a protein known to be also involved into chemo-sensation - was detected in the region of the larval median organ. Moreover, we reveal the presence of an unusual type of photoreceptor as part of the median organ in Idanthyrsus australiensis with a corrugated sensory membrane ultrastructure unlike those observed in the segmental ocelli of other polychaetes. CONCLUSIONS: We are describing for the first time the nuchal organ-like structures in different developmental stages of two species of Sabellariidae. The external morphology, neuronal innervation, developmental fate and ultrastructure of the newly-discovered median organ-based ciliary pits are comparable with the characteristics known for annelid nuchal organs and therefore indicate a homology of both sensory complexes. The presence of myoinhibitory peptide (MIP) in the respective region supports such a hypothesis and exhibits the possibility of an involvement of the entire sabellariid median organ complex, and in particular the prominent ciliated pits, in chemo-sensation.

Behavioural evidence for polychromatic ultraviolet sensitivity in mantis shrimp.

Stomatopod crustaceans are renowned for their elaborate visual systems. Their eyes contain a plethora of photoreceptors specialized for chromatic and polarization detection, including several that are sensitive to varying wavelength ranges and angles of polarization within the ultraviolet (UV) range (less than 400 nm). Behavioural experiments have previously suggested that UV photoreception plays a role in stomatopod communication, but these experiments have only manipulated the entire UV range. Here, using a behavioural approach, we examine UV vision in the stomatopod Haptosquilla trispinosa Using binary trained choice assays as well as innate burrow-choice experiments, we assessed the ability of H. trispinosa to detect and respond to narrow-band LED stimuli peaking near 314 nm (UVB) versus 379 nm (UVA) in wavelength. We find that H. trispinosa can discriminate these stimuli and appears to display an aversive reaction to UVB light, suggesting segregated behavioural responses to stimuli within the UV range. Furthermore, we find that H. trispinosa can discriminate stimuli peaking near 379 nm versus 351 nm in wavelength, suggesting that their wavelength discrimination in the UV is comparable to their performance in the human-visible range.

The sea urchin Diadema africanum uses low resolution vision to find shelter and deter enemies.

Many sea urchins can detect light on their body surface and some species are reported to possess image-resolving vision. Here, we measure the spatial resolution of vision in the long-spined sea urchin Diadema africanum, using two different visual responses: a taxis towards dark objects and an alarm response of spine-pointing towards looming stimuli. For the taxis response we used visual stimuli, which were isoluminant to the background, to discriminate spatial vision from phototaxis. Individual animals were placed in the centre of a cylindrical arena under bright down-welling light, with stimuli of varying angular width placed on the arena wall at alternating directions from the centre. We tracked the direction of movement of individual animals in relation to the stimuli to determine whether the animals oriented towards the stimulus. We found that D. africanum responds by taxis towards isoluminant stimuli with a spatial resolution in the range of 29-69 deg. This corresponds to a theoretical acceptance angle of 38-89 deg, assuming a contrast threshold of 10%. The visual acuity of the alarm response of D. africanum was tested by exposing animals to different sized dark looming and appearing stimuli on a monitor. We found that D. africanum displays a spine-pointing response to appearing black circles of 13-25 deg angular width, corresponding to an acceptance angle of 60-116 deg, assuming the same contrast threshold as above.

Sequence, Structure, and Expression of Opsins in the Monochromatic Stomatopod Squilla empusa.

Most stomatopod crustaceans have complex retinas in their compound eyes, with up to 16 spectral types of photoreceptors, but members of the superfamily Squilloidea have much simpler retinas, thought to contain a single photoreceptor spectral class. In the Atlantic stomatopod Squilla empusa, microspectrophotometry shows that all photoreceptors absorb light maximally at 517 nm, indicating that a single visual pigment is present in all photoreceptors in the retina. However, six distinct, but partial, long wavelength sensitive (LWS) opsin transcripts, which encode the protein component of the visual pigment, have been previously isolated through RT-PCR. In order to investigate the spectral and functional differences among S. empusa's opsins, we used RT-PCR to complete the 3' end of sequences for five of the six expressed opsins. The extended sequences spanned from the first transmembrane (TM1) helix to the 3' end of the coding region. Using homology-based modeling, we predicted the three-dimensional structure of the amino acid translation of the S. empusa opsins. Based on these analyses, S. empusa LWS opsins share a high sequence identity in TM regions and in amino acids within 15 Å of the chromophore-binding lysine on TM helix 7 (TM7), suggesting that these opsins produce spectrally similar visual pigments in agreement with previous results. However, we propose that these spectrally similar opsins differ functionally, as there are non-conservative amino acid substitutions found in intracellular loop 2 (ICL2) and TM5/ICL3, which are critical regions for G-protein binding, and substitutions in extracellular regions suggest different chromophore attachment affinities. In situ hybridization of two of the opsins (Se5 and Se6) revealed strong co-expression in all photoreceptors in both midband and peripheral regions of the retina as well as in selected ocular and cerebral ganglion neuropils. These data suggest the expression of multiple opsins-likely spectrally identical, but functionally different-in multiple types of neuronal cells in S. empusa. This suggests that the multiple opsins characteristic of other stomatopod species may have similar functional specialization.

Radiolar Eyes of Serpulid Worms (Annelida, Serpulidae): Structures, Function, and Phototransduction.

Fan worms, represented by sabellid and serpulid polychaetes, have an astonishing array of unusual eyes and photoreceptors located on their eponymous feeding appendages. Here we organize the previous descriptions of these eyes in serpulids and report new anatomical, molecular, and physiological data regarding their structure, function, and evolution and the likely identity of their phototransduction machinery. We report that, as in sabellids, serpulids display a broad diversity of radiolar eye arrangements and ocellar structures. Furthermore, the visual pigment expressed in the eyes of Spirobranchus corniculatus, a species of the charismatic Christmas tree worms, absorbs light maximally at 464 nm in wavelength. This visual pigment closely matches the spectrum of downwelling irradiance in shallow coral reef habitats and lends support to the hypothesis that these radiolar photoreceptors function as a silhouette-detecting "burglar alarm" that triggers a rapid withdrawal response when the worm is threatened by potential predators. Finally, we report on the transcriptomic sequencing results for the radiolar eyes of S. corniculatus, which express invertebrate c-type opsins in their ciliary radiolar photoreceptors, closely related to the opsin found in the radiolar eyes of the sabellid Acromegalomma interruptum. We explore the potential for a shared evolutionary lineage between the radiolar photoreceptors of serpulids and sabellids and consider these unique innovations in the broader context of metazoan eye evolution.

Crustacean Larvae-Vision in the Plankton.

We review the visual systems of crustacean larvae, concentrating on the compound eyes of decapod and stomatopod larvae as well as the functional and behavioral aspects of their vision. Larval compound eyes of these macrurans are all built on fundamentally the same optical plan, the transparent apposition eye, which is eminently suitable for modification into the abundantly diverse optical systems of the adults. Many of these eyes contain a layer of reflective structures overlying the retina that produces a counterilluminating eyeshine, so they are unique in being camouflaged both by their transparency and by their reflection of light spectrally similar to background light to conceal the opaque retina. Besides the pair of compound eyes, at least some crustacean larvae have a non-imaging photoreceptor system based on a naupliar eye and possibly other frontal eyes. Larval compound-eye photoreceptors send axons to a large and well-developed optic lobe consisting of a series of neuropils that are similar to those of adult crustaceans and insects, implying sophisticated analysis of visual stimuli. The visual system fosters a number of advanced and flexible behaviors that permit crustacean larvae to survive extended periods in the plankton and allows them to reach acceptable adult habitats, within which to metamorphose.

Low-Resolution Vision-at the Hub of Eye Evolution.

Simple roles for photoreception are likely to have preceded more demanding ones such as vision. The driving force behind this evolution is the improvement and elaboration of animal behaviors using photoreceptor input. Because the basic role for all senses aimed at the external world is to guide behavior, we argue here that understanding this "behavioral drive" is essential for unraveling the evolutionary past of the senses. Photoreception serves many different types of behavior, from simple shadow responses to visual communication. Based on minimum performance requirements for different types of tasks, photoreceptors have been argued to have evolved from non-directional receptors, via directional receptors, to low-resolution vision, and finally to high-resolution vision. Through this sequence, the performance requirements on the photoreceptors have gradually changed from broad to narrow angular sensitivity, from slow to fast response, and from low to high contrast sensitivity during the evolution from simple to more advanced and demanding behaviors. New behaviors would only evolve if their sensory performance requirements to some degree overlap with the requirements of already existing behaviors. This need for sensory "performance continuity" must have determined the order by which behaviors have evolved and thus been an important factor guiding animal evolution. Naturally, new behaviors are most likely to evolve from already existing behaviors with similar neural processing needs and similar motor responses, pointing to "neural continuity" as another guiding factor in sensory evolution. Here we use these principles to derive an evolutionary tree for behaviors driven by photoreceptor input.

Phototransduction in fan worm radiolar eyes.

Fan worms (Annelida: Sabellidae) are sessile polychaetes that spend their adult lives in tubes and project their fans, composed of radiolar tentacles, up into the water column for respiration and filter feeding. To protect the fan from predation, many species have evolved unique compound eyes on the radioles that function as shadow or motion detectors, eliciting a rapid withdrawal response in reaction to encroaching objects in the water column [1,2]. The structure of the eyes, their complexity, and their arrangements on the radioles are very diverse among sabellid genera [3] and they display many characteristics atypical of polychaete eyes, such as ciliary photoreceptors [3,4] that hyperpolarize in response to illumination [5]. Here we examine the retinal transcriptome of the radiolar eyes from the fan worm Megalomma interrupta. We find that the opsin, the protein component of light sensitive visual pigments, and other phototransduction cascade signaling proteins expressed in these eyes are related to those commonly associated with vertebrate ciliary photoreceptors, as opposed to the rhabdomeric receptors found in the primary eyes of many invertebrates. With previous anatomical and physiological observations, these results suggest that the radiolar eyes arose independently in fan worms.

Fan worm eyes.

A quick guide to the diverse and unusual eyes of polychaete fan worms, by Michael Bok and Dan-Eric Nilsson.

Photoreception and vision in the ultraviolet.

Ultraviolet (UV) light occupies the spectral range of wavelengths slightly shorter than those visible to humans. Because of its shorter wavelength, it is more energetic (and potentially more photodamaging) than 'visible light', and it is scattered more efficiently in air and water. Until 1990, only a few animals were recognized as being sensitive to UV light, but we now know that a great diversity, possibly even the majority, of animal species can visually detect and respond to it. Here, we discuss the history of research on biological UV photosensitivity and review current major research trends in this field. Some animals use their UV photoreceptors to control simple, innate behaviors, but most incorporate their UV receptors into their general sense of vision. They not only detect UV light but recognize it as a separate color in light fields, on natural objects or living organisms, or in signals displayed by conspecifics. UV visual pigments are based on opsins, the same family of proteins that are used to detect light in conventional photoreceptors. Despite some interesting exceptions, most animal species have a single photoreceptor class devoted to the UV. The roles of UV in vision are manifold, from guiding navigation and orientation behavior, to detecting food and potential predators, to supporting high-level tasks such as mate assessment and intraspecific communication. Our current understanding of UV vision is restricted almost entirely to two phyla: arthropods and chordates (specifically, vertebrates), so there is much comparative work to be done.

Here, There and Everywhere: The Radiolar Eyes of Fan Worms (Annelida, Sabellidae).

Fan worms (Annelida: Sabellidae) possess some of the strangest eyes in nature. Their eponymous fans are composed of two sets of radiolar tentacles that project from the head up out of the worm's protective tube into the water column. Primarily used for respiration and feeding, these radioles are also often involved in photoreception. They display a surprising diversity of eyes of varying levels of sophistication, ranging from scattered single ocelli to compound eyes with up to hundreds of facets. These photoreceptors could represent a relatively recent evolutionary development to cope with a sessile, tube-dwelling lifestyle, and the primary cerebral eyes (haplessly positioned within the tube most of the time) amount to little more than minute pigment cups with scant visual potential. The radiolar eyes on the other hand, appear to function as visual burglar alarms for detecting looming predators and eliciting a startle response for the worm to rapidly retreat within its fortified tube. Despite sometimes resembling arthropod compound eyes, the radiolar photoreceptors have many canonically vertebrate-like physiological characteristics. Considering the unusual and apparently recently evolved nature of the fan worm radiolar photoreceptors, these animals are an excellent case for examining the emergence of novel visual systems, the development of rudimentary visually guided behaviors, and the function of distributed sensory systems. Here, we review over 100 years of investigations into the anatomical diversity of sabellid radiolar photoreceptors and eyes in an evolutionary and functional context. We provide new information on radiolar eye structure in several species of fan worms, and we attempt to organize the various eye types and ocellar structures into meaningful hierarchies. We discuss the developmental, evolutionary, and functional significance of the radiolar eyes and highlight areas of future interest in deciphering their unique nature.