Sea urchins can detect light and move in relation to luminous stimuli despite lacking eyes. They presumably detect light through photoreceptor cells distributed on their body surface. However, there is currently no mechanistic explanation of how these animals can process light to detect visual stimuli and produce oriented movement. Here, we present a model of decentralized vision in echinoderms that includes all known processing stages, from photoreceptor cells to radial nerve neurons to neurons contained in the oral nerve ring encircling the mouth of the animals. In the model, light stimuli captured by photoreceptor cells produce neural activity in the radial nerve neurons. In turn, neural activity in the radial nerves is integrated in the oral nerve ring to produce a profile of neural activity reaching spatially across several ambulacra. This neural activity is read out to produce a model of movement. The model captures the pattern of behavior observed in sea urchin Diadema africanum probed with a variety of physical stimuli. The specific pattern of neural connections used in the model makes testable predictions on the properties of single neurons and aggregate neural behavior in Diadema africanum and other echinoderms, offering a potential understanding of the mechanism of visual orientation in these animals.

Spatial vision was recently reported in a brittle star, Ophiomastix wendtii, which lacks discrete eyes, but little is known about its visual ecology. Our aim was to better characterize the vision and visual ecology of this unusual visual system. We tested animals’ orientation relative to vertical bar stimuli at a range of angular widths and contrast, to identify limits of angular and contrast detection. We also presented dynamic shadow stimuli, either looming towards or passing overhead the animal, to test for potential defensive responses. Finally, we presented animals lacking a single arm with a vertical bar stimulus known to elicit a response in intact animals. We found that O. wendtii orients to large ($≥$50° ), high-contrast vertical bar stimuli, consistent with a shelter-seeking role and with photoreceptor acceptance angles estimated from morphology. We calculate poor optical sensitivity for individual photoreceptors, and predict dramatic oversampling for photoreceptor arrays. We also report responses to dark stimuli moving against a bright background - this is the first report of responses to moving stimuli in brittle stars and suggests additional defensive uses for vision in echinoderms. Finally, we found that animals missing a single arm orient worse to static stimuli, which requires further investigation.

How well can a bird discriminate between two red berries on a green background? The absolute threshold of colour discrimination is set by photoreceptor noise, but animals do not perform at this threshold; their performance can depend on additional factors. In humans and zebra finches, discrimination thresholds for colour stimuli depend on background colour, and thus the adaptive state of the visual system. We have tested how well chickens can discriminate shades of orange or green presented on orange or green backgrounds. Chickens discriminated slightly smaller colour differences between two stimuli presented on a similarly coloured background, compared with a background of very different colour. The slope of the psychometric function was steeper when stimulus and background colours were similar but shallower when they differed markedly, indicating that background colour affects the certainty with which the animals discriminate the colours. The effect we find for chickens is smaller than that shown for zebra finches. We modelled the response to stimuli using Bayesian and maximum likelihood estimation and implemented the psychometric function to estimate the effect size. We found that the result is independent of the psychophysical method used to evaluate the effect of experimental conditions on choice performance.

Almost all animals can sense light, but only those with spatial vision can ‘‘see.’’ Conventionally, this was restricted to animals possessing discrete visual organs (eyes), but extraocular vision could facilitate vision without eyes. Echinoderms form the focus of extraocular vision research [1–7], and the brittle star Ophiocoma wendtii, which exhibits light-responsive color change and shelter seeking, became a key species of interest [4, 8, 9]. Both O. wendtii and an apparently light-indifferent congeneric, O. pumila, possess an extensive network of r-opsin-reactive cells, but its function remains unclear [4]. We show that, although both species are strongly light averse, O. wendtii orients to stimuli necessitating spatial vision for detection, but O. pumila does not. However, O. wendtii’s response disappears when chromatophores are contracted within the skeleton. Combining immunohistochemistry, histology, and synchrotron microtomography, we reconstructed models of photoreceptors in situ and extracted estimated angular apertures for O. wendtii and O. pumila. Angular sensitivity estimates, derived from these models, support the hypothesis that chromatophores constitute a screening mechanism in O. wendtii, providing sufficient resolving power to detect the stimuli. RNA sequencing (RNA-seq) identified opsin candidates in both species, including multiple r-opsins and transduction pathway constituents, congruent with immunohistochemistry and studies of other echinoderms [10, 11]. Finally, we note that differing body postures between the two species during experiments may reflect aspect of signal integration. This represents one of the most detailed mechanisms for extraocular vision yet proposed and draws interesting parallels with the only other confirmed extraocular visual system, that of some sea urchins, which also possess chromatophores.

Millipedes are a species-rich and ancient arthropod clade which typically bear a pair of lateral compound eyes with a small number of large facets. To understand the visual tasks that underlie the evolution of millipede eyes, their spatial resolving performance is of key importance. We here investigate the spatial resolution of the millipede Cylindroiulus punctatus using behavioural assays. Individual animals were placed in the centre of a cylindrical arena under bright downwelling light, with dark stimuli of varying angular dimensions placed on the arena wall. We used continuous isoluminant stimuli based on a difference of Gaussians signal to test for orientation to the dark target via object taxis. Headings of individual animals were tracked in relation to the stimuli to determine whether the animals oriented towards the stimulus. We implemented a multilevel logistic regression model to identify the arc width of the stimulus that animals could resolve. We then modelled the angular sensitivity needed to identify this. We also related the visual performance to the 3D anatomy of the eye. We found that C. punctatus can resolve a stimulus of 56° period (sufficient to detect a 20° dark target). Assuming a contrast threshold of 10%, this requires a receptor acceptance angle of 72° or narrower. Spatial resolving power this low would only suffice for the simplest visual tasks, such as shelter-seeking.

For polarized light to inform behaviour, the typical range of degrees of polarization observable in the animal’s natural environment must be above the threshold for detection and interpretation. Here, we present the first investigation of the degree of linear polarization threshold for orientation behaviour in a nocturnal species, with specific reference to the range of degrees of polarization measured in the night sky. An effect of lunar phase on the degree of polarization of skylight was found, with smaller illuminated fractions of the moon’s surface corresponding to lower degrees of polarization in the night sky. We found that the South African dung beetle Escarabaeus satyrus can orient to polarized light for a range of degrees of polarization similar to that observed in diurnal insects, reaching a lower threshold between 0.04 and 0.32, possibly as low as 0.11. For degrees of polarization lower than 0.23, as measured on a crescent moon night, orientation performance was considerably weaker than that observed for completely linearly polarized stimuli, but was nonetheless stronger than in the absence of polarized light.

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.

Skip to Next Section Onychophorans, also known as velvet worms, possess a pair of simple lateral eyes, and are a key lineage with regard to the evolution of vision. They resemble ancient Cambrian forms, and are closely related to arthropods, which boast an unrivalled diversity of eye designs. Nonetheless, the visual capabilities of onychophorans have not been well explored. Here, we assessed the spatial resolution of the onychophoran Euperipatoides rowelli using behavioural experiments, three-dimensional reconstruction, anatomical and optical examinations, and modelling. Exploiting their spontaneous attraction towards dark objects, we found that E. rowelli can resolve stimuli that have the same average luminance as the background. Depending on the assumed contrast sensitivity of the animals, we estimate the spatial resolution to be in the range 15–40 deg. This results from an arrangement where the cornea and lens project the image largely behind the retina. The peculiar ellipsoid shape of the eye in combination with the asymmetric position and tilted orientation of the lens may improve spatial resolution in the forward direction. Nonetheless, the unordered network of interdigitating photoreceptors, which fills the whole eye chamber, precludes high-acuity vision. Our findings suggest that adult specimens of E. rowelli cannot spot or visually identify prey or conspecifics beyond a few centimetres from the eye, but the coarse spatial resolution that the animals exhibited in our experiments is likely to be sufficient to find shelter and suitable microhabitats from further away. To our knowledge, this is the first evidence of resolving vision in an onychophoran.

Light-detection provides incomparabaly rapid information at a range of time scales and, consequently, directional photoreception is found in almost every major metazoan clade. Conversely, a much smaller cohort have evolved sophisticated high resolution vision, which facillitates complex tasks via the detection of fast or small objects,. such as courtship and high-speed pursuit of prey. A few such species are the focus of most vision research. In contrast, low resolution image-forming vision is little investigated and, in some cases, whether vision is present has not been directly evidenced. To ameliorate this, I tested the image-forming capability (spatial resolution) of a variety of eye types from diverse animal groups: the camera eye of a velvet worm, Euperipatoides rowelli, (paper I), the dispersed visual system of a diadematid sea urchin, Diadema africanum, (paper II), which lacks discrete eyes, the cup eye of a planarian flatworm, Schmidtea lugubris, (paper III) and the compound eye of a millipede, Cylindroiulus punctatus, (paper IV). For each study animal, I used behavioural experiments in which the animals responded to dark visual cues to test whether they could response to visual stimuli of different sizes. The animals were placed in circular arenas under bright light and the direction they moved in relation to the stimulus was recorded. As a negative phototaxis response is present in each species, attraction towards the stimulus, if it could be resolved provided a measure of resolution. The angular sensitivity of an eye required to see a given visual signal was modelled (making assumptions about their contrast sensitivity; discussed in paper I).. I compared the efficacy of the various visual stimulus types for this purpose in paper II. To account for mutiple effects and low response rates to stimuli I apply logistic regression models using Bayesian inference in papers III and IV , to make more robust estimates which better express uncertainty. I also used imaging techniques, including x-ray tomography and transmission electron microscopy, to relate the visual performance of these animals to their visual systems. We found that these animals each had coarse vision with a spatial resolution of 20-30° to for the velvet worm E. rowelli, 29-69° for the sea urchin D. africanum (in respect of object taxis), 63° for the millipede C. punctatus and 73° for the flatworm S. lugubris. These modest proposed ranges of spatial resolution are nonetheless sufficient for the visual tasks employed by these animals.

Recent findings of sequence convergence in the Prestin gene among some bats and cetaceans suggest that parallel adaptations for high-frequency hearing have taken place during the evolution of echolocation. To determine if this gene is an exception, or instead similar processes have occurred in other hearing genes, we have examined Tmc1 and Pjvk, both of which are associated with non-syndromic hearing loss in mammals. These genes were amplified and sequenced from a number of mammalian species, including echolocating and non-echolocating bats and whales, and were analysed together with published sequences. Sections of both genes showed phylogenetic signals that conflicted with accepted species relationships, with coding regions uniting laryngeal echolocating bats in a monophyletic clade. Bayesian estimates of posterior probabilities of convergent and divergent substitutions provided more direct evidence of sequence convergence between the two groups of laryngeal echolocating bats as well as between echolocating bats and dolphins. We found strong evidence of positive selection acting on some echolocating bat species and echolocating cetaceans, contrasting with purifying selection on non-echolocating bats. Signatures of sequence convergence and molecular adaptation in two additional hearing genes suggest that the acquisition of high-frequency hearing has involved multiple loci.