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'.

Strange eyes, stranger brains: exceptional diversity of optic lobe organization in midwater crustaceans.

Nervous systems across Animalia not only share a common blueprint at the biophysical and molecular level, but even between diverse groups of animals the structure and neuronal organization of several brain regions are strikingly conserved. Despite variation in the morphology and complexity of eyes across malacostracan crustaceans, many studies have shown that the organization of malacostracan optic lobes is highly conserved. Here, we report results of divergent evolution to this 'neural ground pattern' discovered in hyperiid amphipods, a relatively small group of holopelagic malacostracan crustaceans that possess an unusually wide diversity of compound eyes. We show that the structure and organization of hyperiid optic lobes has not only diverged from the malacostracan ground pattern, but is also highly variable between closely related genera. Our findings demonstrate a variety of trade-offs between sensory systems of hyperiids and even within the visual system alone, thus providing evidence that selection has modified individual components of the central nervous system to generate distinct combinations of visual centres in the hyperiid optic lobes. Our results provide new insights into the patterns of brain evolution among animals that live under extreme conditions.

Mantis shrimp identify an object by its shape rather than its color during visual recognition.

Mantis shrimp commonly inhabit seafloor environments with an abundance of visual features including conspecifics, predators, prey and landmarks used for navigation. Although these animals are capable of discriminating color and polarization, it is unknown what specific attributes of a visual object are important during recognition. Here, we show that mantis shrimp of the species Neogonodactylus oerstedii are able to learn the shape of a trained target. Further, when the shape and color of a target that they had been trained to identify were placed in conflict, N. oerstedii tended to choose the target of the trained shape over the target of the trained color. Thus, we conclude that the shape of the target was more salient than its color during recognition by N. oerstedii, suggesting that the shapes of objects, such as landmarks or other animals, are important for their identification by the species.

Visual system characterization of the obligate bat ectoparasite Trichobius frequens (Diptera: Streblidae).

As an obligate ectoparasite of bats, the bat fly Trichobius frequens (Diptera: Streblidae) inhabits the same subterranean environment as their nocturnal bat hosts. In this study, we characterize the macromorphology, optical architecture, rhabdom anatomy, photoreceptor absorbance, and opsin expression of the significantly reduced visual system in T. frequens resulting from evolution in the dark. The eyes develop over a 21-22 day pupal developmental period, with pigmentation appearing on pupal day 11. After eclosion as an adult, T. frequens eyes consist of on average 8 facets, each overlying a fused rhabdom consisting of anywhere from 11 to 18 estimated retinula cells. The dimensions of the facets and fused rhabdoms are similar to those measured in other nocturnal insects. T. frequens eyes are functional as shown by expression of a Rh1 opsin forming a visual pigment with a peak sensitivity to 487 nm, similar to other dipteran Rh1 opsins. Future studies will evaluate how individuals with such reduced capabilities for spatial vision as well as sensitivity still capture enough visual information to use flight to maneuver through dark habitats.

Landmark navigation in a mantis shrimp.

Mantis shrimp commonly occupy burrows in shallow, tropical waters. These habitats are often structurally complex where many potential landmarks are available. Mantis shrimp of the species Neogonodactylus oerstedii return to their burrows between foraging excursions using path integration, a vector-based navigational strategy that is prone to accumulated error. Here, we show that N. oerstedii can navigate using landmarks in parallel with their path integration system, correcting for positional uncertainty generated when navigating using solely path integration. We also report that when the path integration and landmark navigation systems are placed in conflict, N. oerstedii will orientate using either system or even switch systems enroute. How they make the decision to trust one navigational system over another is unclear. These findings add to our understanding of the refined navigational toolkit N. oerstedii relies upon to efficiently navigate back to its burrow, complementing its robust, yet error prone, path integration system with landmark guidance.

Visual metamorphoses in insects and malacostracans: Transitions between an aquatic and terrestrial life.

Arthropods operate in an outrageous diversity of environments. From the deep sea to dense tropical forests, to wide open arctic tundra, they have colonized almost every possible habitat. Within these environments, the presence of light is nearly ubiquitous, varying in intensity, wavelength, and polarization. Light provides critical information about the environment, such as time of day or where food sources may be located. Animals take advantage of this prevalent and informative cue to make behavioral choices. However, the types of choices animals face depend greatly on their environments and needs at any given time. In particular, animals that undergo metamorphosis, with arthropods being the prime example, experience dramatic changes in both behavior and ecology, which in turn may require altering the structure and function of sensory systems such as vision. Amphibiotic organisms maintain aquatic lifestyles as juveniles before transitioning to terrestrial lifestyles as adults. However, light behaves differently in water than in air, resulting in distinct aquatic and terrestrial optical environments. Visual changes in response to these optical differences can occur on multiple levels, from corneal structure down to neural organization. In this review, we summarize examples of alterations in the visual systems of amphibiotic larval and adult insects and malacostracan crustaceans, specifically those attributed to environmental differences between metamorphic phases.

Sensory Ecology: In Sea Snake Vision, One Plus One Makes Three.

Snake genomes encode only two opsins for use in retinal cones, limiting their adaptive flexibility and color vision. Research now shows that, by using alternative opsin alleles, some sea snakes may add a third opsin spectral class to their retinas.

Path integration error and adaptable search behaviors in a mantis shrimp.

Mantis shrimp of the species Neogonodactylus oerstedii occupy small burrows in shallow waters throughout the Caribbean. These animals use path integration, a vector-based navigation strategy, to return to their homes while foraging. Here, we report that path integration in N. oerstedii is prone to error accumulated during outward foraging paths and we describe the search behavior that N. oerstedii employs after it fails to locate its home following the route provided by its path integrator. This search behavior forms continuously expanding, non-oriented loops that are centered near the point of search initiation. The radius of this search is scaled to the animal's positional uncertainty during path integration, improving the effectiveness of the search. The search behaviors exhibited by N. oerstedii bear a striking resemblance to search behaviors in other animals, offering potential avenues for the comparative examination of search behaviors and how they are optimized in disparate taxa.

Mantis Shrimp Navigate Home Using Celestial and Idiothetic Path Integration.

Path integration is a robust mechanism that many animals employ to return to specific locations, typically their homes, during navigation. This efficient navigational strategy has never been demonstrated in a fully aquatic animal, where sensory cues used for orientation may differ dramatically from those available above the water's surface. Here, we report that the mantis shrimp, Neogonodactylus oerstedii, uses path integration informed by a hierarchical reliance on the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging, making them the first fully aquatic path-integrating animals yet discovered. We show that mantis shrimp rely on navigational strategies closely resembling those used by insect navigators, opening a new avenue for the investigation of the neural basis of navigation behaviors and the evolution of these strategies in arthropods and potentially other animals as well. VIDEO ABSTRACT.

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.

Optic lobe organization in stomatopod crustacean species possessing different degrees of retinal complexity.

Stomatopod crustaceans possess tripartite compound eyes; upper and lower hemispheres are separated by an equatorial midband of several ommatidial rows. The organization of stomatopod retinas is well established, but their optic lobes have been studied less. We used histological staining, immunolabeling, and fluorescent tracer injections to compare optic lobes in two 6-row midband species, Neogonodactylus oerstedii and Pseudosquilla ciliata, to those in two 2-row midband species, Squilla empusa and Alima pacifica. Compared to the 6-row species, we found structural differences in all optic neuropils in both 2-row species. Photoreceptor axons from 2-row midband ommatidia supply two sets of lamina cartridges; however, conspicuous spaces lacking lamina cartridges are observed in locations corresponding to where the cartridges of the upper four ommatidial rows of 6-row species would exist. The tripartite arrangement and enlarged projections containing fibers associated with the two rows of midband ommatidia can be traced throughout the entire optic lobe. However, 2-row species lack some features of medullar and lobular neuropils in 6-row species. Our results support the hypothesis that 2-row midband species are derived from a 6-row ancestor, and suggest specializations in the medulla and lobula found solely in 6-row species are important for color and polarization analysis.

Vision in the snapping shrimp Alpheus heterochaelis.

Snapping shrimp engage in heterospecific behavioral associations in which their partners, such as goby fish, help them avoid predators. It has been argued that snapping shrimp engage in these partnerships because their vision is impaired by their orbital hood, an extension of their carapace that covers their eyes. To examine this idea, we assessed the visual abilities of snapping shrimp. We found the big claw snapping shrimp, Alpheus heterochaelis, has spatial vision provided by compound eyes with reflecting superposition optics. These eyes view the world through an orbital hood that is 80-90% as transparent as seawater across visible wavelengths (400-700 nm). Through electroretinography and microspectrophotometry, we found the eyes of A. heterochaelis have a temporal sampling rate of >40 Hz and have at least two spectral classes of photoreceptors (λmax=500 and 519 nm). From the results of optomotor behavioral experiments, we estimate the eyes of A. heterochaelis provide spatial vision with an angular resolution of ∼8 deg. We conclude that snapping shrimp have competent visual systems, suggesting the function and evolution of their behavioral associations should be re-assessed and that these animals may communicate visually with conspecifics and heterospecific partners.

Long-Wavelength Reflecting Filters Found in the Larval Retinas of One Mantis Shrimp Family (Nannosquillidae).

Both vertebrates and invertebrates commonly exploit photonic structures adjacent to their photoreceptors for visual benefits. For example, use of a reflecting structure (tapetum) behind the retina increases photon capture, enhancing vision in dim light [1-5]. Colored filters positioned lateral or distal to a photoreceptive unit may also be used to tune spectral sensitivity by selective transmission of wavelengths not absorbed or scattered by the filters [6-8]. Here we describe a new category of biological optical filter that acts simultaneously as both a transmissive spectral filter and narrowband reflector. Discovered in the larval eyes of only one family of mantis shrimp (stomatopod) crustaceans (Nannosquillidae), each crystalline structure bisects the photoreceptive rhabdom into two tiers and contains an ordered array of membrane-bound vesicles with sub-wavelength diameters of 153 ± 5 nm. Axial illumination of the intrarhabdomal structural reflector (ISR) in vivo produces a narrow band of yellow reflectance (mean peak reflectivity, 572 ± 18 nm). The ISR is similar to several synthetic devices, such as bandgap filters, laser mirrors, and (in particular) fiber Bragg gratings used in optical sensors for a wide range of industries. To our knowledge, the stomatopod larval ISR is the first example of a naturally occurring analog to these human-made devices. Considering what is known about these animals' visual ecology, we propose that these reflecting filters may help improve the detection of pelagic bioluminescence in shallow water at night. VIDEO ABSTRACT.

Polarisation signals: a new currency for communication.

Most polarisation vision studies reveal elegant examples of how animals, mainly the invertebrates, use polarised light cues for navigation, course-control or habitat selection. Within the past two decades it has been recognised that polarised light, reflected, blocked or transmitted by some animal and plant tissues, may also provide signals that are received or sent between or within species. Much as animals use colour and colour signalling in behaviour and survival, other species additionally make use of polarisation signalling, or indeed may rely on polarisation-based signals instead. It is possible that the degree (or percentage) of polarisation provides a more reliable currency of information than the angle or orientation of the polarised light electric vector (e-vector). Alternatively, signals with specific e-vector angles may be important for some behaviours. Mixed messages, making use of polarisation and colour signals, also exist. While our knowledge of the physics of polarised reflections and sensory systems has increased, the observational and behavioural biology side of the story needs more (and more careful) attention. This Review aims to critically examine recent ideas and findings, and suggests ways forward to reveal the use of light that we cannot see.

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.

A different view: sensory drive in the polarized-light realm.

Sensory drive, the concept that sensory systems primarily evolve under the influence of environmental features and that animal signals are evolutionarily shaped and tuned by these previously existing sensory systems, has been thoroughly studied regarding visual signals across many animals. Much of this work has focused on spectral aspects of vision and signals. Here, I review work on polarized-light signals of animals and relate these to what is known of polarization visual systems, polarized-light aspects of visual scenes, and polarization-related behavior (e.g., orientation, habitat-finding, contrast enhancement). Other than the broad patterns of scattered polarized light in the sky, most polarization in both terrestrial and aquatic environments results from either reflection or scattering in the horizontal plane. With overhead illumination, horizontal features such as the surfaces of many leaves or of air: water interfaces reflect horizontal polarization, and water scatters horizontally polarized light under most conditions. Several animal species have been demonstrated to use horizontally polarized light fields or features in critical aspects of their biology. Significantly, most biological signals are also horizontally polarized. Here, I present relevant polarization-related behavior and discuss the hypothesis that sensory drive has evolutionarily influenced the structure of polarization signals. The paper also considers the evolutionary origin of circular polarization vision and circularly polarized signals. It appears that this class of signals did not evolve under the influence of sensory drive. The study of signals based on polarized light is becoming a mature field of research.

Cerebral photoreception in mantis shrimp.

The currently unsurpassed diversity of photoreceptors found in the eyes of stomatopods, or mantis shrimps, is achieved through a variety of opsin-based visual pigments and optical filters. However, the presence of extraocular photoreceptors in these crustaceans is undescribed. Opsins have been found in extraocular tissues across animal taxa, but their functions are often unknown. Here, we show that the mantis shrimp Neogonodactylus oerstedii has functional cerebral photoreceptors, which expands the suite of mechanisms by which mantis shrimp sense light. Illumination of extraocular photoreceptors elicits behaviors akin to common arthropod escape responses, which persist in blinded individuals. The anterior central nervous system, which is illuminated when a mantis shrimp's cephalothorax protrudes from its burrow to search for predators, prey, or mates, appears to be photosensitive and to feature two types of opsin-based, potentially histaminergic photoreceptors. A pigmented ventral eye that may be capable of color discrimination extends from the cerebral ganglion, or brain, against the transparent outer carapace, and exhibits a rapid electrical response when illuminated. Additionally, opsins and histamine are expressed in several locations of the eyestalks and cerebral ganglion, where any photoresponses could contribute to shelter-seeking behaviors and other functions.

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.

Multichannel spectrometers in animals.

Multispectral, hyperspectral, polarimetric, and other types of multichannel imaging spectrometers are coming into common use for a variety of applications, including remote sensing, material identification, forensics, and medical diagnosis. These instruments are often bulky and intolerant of field abuse, so designing compact, reliable, portable, and robust devices is a priority. In contrast to most engineering designs, animals have been building compact and robust multichannel imaging systems for millennia-their eyes. Biological sensors arise by evolution, of course, and are not designed 'for' a particular use; they exist because the creatures that were blessed with useful mutations were better able to survive and reproduce than their competitors. While this is an inefficient process for perfecting a sensor, it brings unexpected innovations and novel concepts into visual system design-concepts that may be useful in the inspiration of new engineered solutions to problematic challenges, like the ones mentioned above. Here, we review a diversity of multichannel visual systems from both vertebrate and invertebrate animals, considering the receptor molecules and cells, spectral sensitivity and its tuning, and some aspects of the higher-level processing systems used to shape spectral (and polarizational) channels in vision. The eyes of mantis shrimps are presented as potential models for biomimetic multichannel imaging systems. We end with a description of a bioinspired, newly developed multichannel spectral/polarimetric imaging system based on mantis shrimp vision that is highly adaptable to field application.

Two visual systems in one eyestalk: The unusual optic lobe metamorphosis in the stomatopod Alima pacifica.

The compound eyes of adult stomatopod crustaceans have two to six ommatidial rows at the equator, called the midband, that are often specialized for color and polarization vision. Beneath the retina, this midband specialization is represented as enlarged optic lobe lamina cartridges and a hernia-like expansion in the medulla. We studied how the optic lobe transforms from the larvae, which possess typical crustacean larval compound eyes without a specialized midband, through metamorphosis into the adults with the midband in a two midband-row species Alima pacifica. Using histological staining, immunolabeling, and 3D reconstruction, we show that the last-stage stomatopod larvae possess double-retina eyes, in which the developing adult visual system forms adjacent to, but separate from, the larval visual system. Beneath the two retinas, the optic lobe also contains two sets of optic neuropils, comprising of a larval lamina, medulla, and lobula, as well as an adult lamina, medulla, and lobula. The larval eye and all larval optic neuropils degenerate and disappear approximately a week after metamorphosis. In stomatopods, the unique adult visual system and all optic neuropils develop alongside the larval system in the eyestalk of last-stage larvae, where two visual systems and two independent visual processing pathways coexist. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 3-14, 2018.