Anders Garm

Advanced optics in a jellyfish eye.

Cubozoans, or box jellyfish, differ from all other cnidarians by an active fish-like behaviour and an elaborate sensory apparatus. Each of the four sides of the animal carries a conspicuous sensory club (the rhopalium), which has evolved into a bizarre cluster of different eyes. Two of the eyes on each rhopalium have long been known to resemble eyes of higher animals, but the function and performance of these eyes have remained unknown. Here we show that box-jellyfish lenses contain a finely tuned refractive index gradient producing nearly aberration-free imaging. This demonstrates that even simple animals have been able to evolve the sophisticated visual optics previously known only from a few advanced bilaterian phyla. However, the position of the retina does not coincide with the sharp image, leading to very wide and complex receptive fields in individual photoreceptors. We argue that this may be useful in eyes serving a single visual task. The findings indicate that tailoring of complex receptive fields might have been one of the original driving forces in the evolution of animal lenses.

Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie

SUMMARY Box jellyfish, cubomedusae, possess an impressive total of 24 eyes of four morphologically different types. Two of these eye types, called the upper and lower lens eyes, are camera-type eyes with spherical fish-like lenses. Compared with other cnidarians, cubomedusae also have an elaborate behavioral repertoire, which seems to be predominantly visually guided. Still, positive phototaxis is the only behavior described so far that is likely to be correlated with the eyes. We have explored the obstacle avoidance response of the Caribbean species Tripedalia cystophora and the Australian species Chiropsella bronzie in a flow chamber. Our results show that obstacle avoidance is visually guided. Avoidance behavior is triggered when the obstacle takes up a certain angle in the visual field. The results do not allow conclusions on whether color vision is involved but the strength of the response had a tendency to follow the intensity contrast between the obstacle and the surroundings (chamber walls). In the flow chamber Tripedalia cystophora displayed a stronger obstacle avoidance response than Chiropsella bronzie since they had less contact with the obstacles. This seems to follow differences in their habitats.

Box Jellyfish Use Terrestrial Visual Cues for Navigation

Box jellyfish have an impressive set of 24 eyes of four different types, including eyes structurally similar to those of vertebrates and cephalopods [1, 2]. However, the known visual responses are restricted to simple phototaxis, shadow responses, and object avoidance responses [3-8], and it has been a puzzle why they need such a complex set of eyes. Here we report that medusae of the box jellyfish Tripedalia cystophora are capable of visually guided navigation in mangrove swamps using terrestrial structures seen through the water surface. They detect the mangrove canopy by an eye type that is specialized to peer up through the water surface and that is suspended such that it is constantly looking straight up, irrespective of the orientation of the jellyfish. The visual information is used to navigate to the preferred habitat at the edge of mangrove lagoons.

The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant)

SUMMARY Box jellyfish, or cubomedusae (class Cubozoa), are unique among the Cnidaria in possessing lens eyes similar in morphology to those of vertebrates and cephalopods. Although these eyes were described over 100 years ago, there has been no work done on their electrophysiological responses to light. We used an electroretinogram (ERG) technique to measure spectral sensitivity of the lens eyes of the Caribbean species Tripedalia cystophora. The cubomedusae have two kinds of lens eyes, the lower and upper lens eyes. We found that both lens eye types have similar spectral sensitivities, which likely result from the presence of a single receptor type containing a single opsin. The peak sensitivity is to blue-green light. Visual pigment template fits indicate a vitamin A-1 based opsin with peak sensitivity near 500 nm for both eye types.

Using phylogenetically-informed annotation (PIA) to search for light-interacting genes in transcriptomes from non-model organisms

BackgroundTools for high throughput sequencing and de novo assembly make the analysis of transcriptomes (i.e. the suite of genes expressed in a tissue) feasible for almost any organism. Yet a challenge for biologists is that it can be difficult to assign identities to gene sequences, especially from non-model organisms. Phylogenetic analyses are one useful method for assigning identities to these sequences, but such methods tend to be time-consuming because of the need to re-calculate trees for every gene of interest and each time a new data set is analyzed. In response, we employed existing tools for phylogenetic analysis to produce a computationally efficient, tree-based approach for annotating transcriptomes or new genomes that we term Phylogenetically-Informed Annotation (PIA), which places uncharacterized genes into pre-calculated phylogenies of gene families.ResultsWe generated maximum likelihood trees for 109 genes from a Light Interaction Toolkit (LIT), a collection of genes that underlie the function or development of light-interacting structures in metazoans. To do so, we searched protein sequences predicted from 29 fully-sequenced genomes and built trees using tools for phylogenetic analysis in the Osiris package of Galaxy (an open-source workflow management system). Next, to rapidly annotate transcriptomes from organisms that lack sequenced genomes, we repurposed a maximum likelihood-based Evolutionary Placement Algorithm (implemented in RAxML) to place sequences of potential LIT genes on to our pre-calculated gene trees. Finally, we implemented PIA in Galaxy and used it to search for LIT genes in 28 newly-sequenced transcriptomes from the light-interacting tissues of a range of cephalopod mollusks, arthropods, and cubozoan cnidarians. Our new trees for LIT genes are available on the Bitbucket public repository (http://bitbucket.org/osiris_phylogenetics/pia/) and we demonstrate PIA on a publicly-accessible web server (http://galaxy-dev.cnsi.ucsb.edu/pia/).ConclusionsOur new trees for LIT genes will be a valuable resource for researchers studying the evolution of eyes or other light-interacting structures. We also introduce PIA, a high throughput method for using phylogenetic relationships to identify LIT genes in transcriptomes from non-model organisms. With simple modifications, our methods may be used to search for different sets of genes or to annotate data sets from taxa outside of Metazoa.

Visual navigation in starfish: first evidence for the use of vision and eyes in starfish

Most known starfish species possess a compound eye at the tip of each arm, which, except for the lack of true optics, resembles an arthropod compound eye. Although these compound eyes have been known for about two centuries, no visually guided behaviour has ever been directly associated with their presence. There are indications that they are involved in negative phototaxis but this may also be governed by extraocular photoreceptors. Here, we show that the eyes of the coral-reef-associated starfish Linckia laevigata are slow and colour blind. The eyes are capable of true image formation although with low spatial resolution. Further, our behavioural experiments reveal that only specimens with intact eyes can navigate back to their reef habitat when displaced, demonstrating that this is a visually guided behaviour. This is, to our knowledge, the first report of a function of starfish compound eyes. We also show that the spectral sensitivity optimizes the contrast between the reef and the open ocean. Our results provide an example of an eye supporting only low-resolution vision, which is believed to be an essential stage in eye evolution, preceding the high-resolution vision required for detecting prey, predators and conspecifics.

Structure and optics of the eyes of the box jellyfish Chiropsella bronzie

Cubomedusae have a total of 24 eyes of four morphologically different types. Two of these eye types are camera-type eyes (upper and lower lens-eye), while the other two eye types are simpler pigment pit eyes (pit and slit eye). Here, we give a description of the visual system of the box jellyfish species Chiropsella bronzie and the optics of the lens eyes in this species. One aim of this study is to distinguish between general cubozoan features and species-specific features in the layout and optics of the eyes. We find that both types of lens eyes are more severely under-focused in C. bronzie than those in the previously investigated species Tripedalia cystophora. In the lower lens-eye of C. bronzie, blur circles subtend 20 and 52° for closed and open pupil, respectively, effectively removing all but the coarsest structures of the image. Histology reveals that the retina of the lower lens-eye, in addition to pigmented photoreceptors, also contains long pigment-cells, with both dark and white pigment, where the dark pigment migrates on light/dark adaptation. Unlike the upper lens-eye lens of T.cystophora, the same eye in C.bronzie did not display any significant optical power.

Function and Functional Groupings of the Complex Mouth Apparatus of the Squat Lobsters Munida sarsi Huus and M. tenuimana G.O. Sars (Crustacea: Decapoda)

Like all other decapods, the anomuran squat lobsters Munida sarsi and M. tenuimana have a mouth apparatus composed of six pairs of mouthparts plus labrum and paragnaths (upper and lower lips). To study the functional significance of this complexity, we examined the mouthparts with scanning electron microscopy and also observed their function directly, under laboratory conditions, using macro-video equipment. No differences were found between the two species. The movement patterns of the mouthparts are described in detail and illustrated as serial drawings. Proceeding from maxillipeds 3 towards the mandibles, the movement pattern gets increasingly stereotypical, with the mandibles performing but a single movement in a medio-lateral plane. From morphology, the mouthparts are subdivided into 20 parts, but from the functional analyses the 20 parts form 8 functional groups: 1, transporting mouthparts (maxilliped 2 endopod and maxilliped 3 endopod); 2, transporting–aligning mouthparts (maxilliped 1 basis); 3, sorting–aligning mouthparts (maxilla 1 basis and maxilla 2 basis); 4, current–generating mouthparts (flagella of maxilliped 2 and maxilliped 3 exopods); 5, cutting–crushing mouthparts (incisor and molar processes, labium, and mandibular palp); 6, ingesting mouthparts (maxilla 1 coxa, maxilla 2 coxa, and maxilliped 1 coxa); 7, respiratory mouthparts (scaphognathite, maxilliped 1 epipod, and maxilliped 2 and maxilliped 3 exopods); and 8, dorso-ventral mouthparts (maxilla 1 endopod, maxilla 2 endopod, maxilliped 1 endopod, and maxilliped 1 exopod). These groupings apply mostly to the processes of food handling and have little significance with respect to grooming. When comparing our results to the literature on other decapods, we found much resemblance to conditions in other anomurans.

Visual control of steering in the box jellyfish Tripedalia cystophora

SUMMARY Box jellyfish carry an elaborate visual system consisting of 24 eyes, which they use for driving a number of behaviours. However, it is not known how visual input controls the swimming behaviour. In this study we exposed the Caribbean box jellyfish Tripedalia cystophora to simple visual stimuli and recorded changes in their swimming behaviour. Animals were tethered in a small experimental chamber, where we could control lighting conditions. The behaviour of the animals was quantified by tracking the movements of the bell, using a high-speed camera. We found that the animals respond predictably to the darkening of one quadrant of the equatorial visual world by (1) increasing pulse frequency, (2) creating an asymmetry in the structure that constricts the outflow opening of the bell, the velarium, and (3) delaying contraction at one of the four sides of the bell. This causes the animals to orient their bell in such a way that, if not tethered, they would turn and swim away from the dark area. We conclude that the visual system of T. cystophora has a predictable effect on swimming behaviour.

Mechanosensory neurons with bend- and osmo-sensitivity in mouthpart setae from the spiny lobster Panulirus argus

The mouthparts of the spiny lobster Panulirus argus hold primarily two types of setae—simple setae and cuspidate setae. Mechanosensory neurons from these setae were examined by electrophysiological recordings. The population of simple setae contained two types of mechanosensory neurons: displacement-sensitive neurons, which responded to deflection at the setal base; and bend-sensitive neurons, which responded to bending of the setal shaft. Displacement-sensitive neurons, in general, responded phasically and only during actual displacement. Typically, their response changed with alteration of the direction, amplitude, and velocity/acceleration of the mechanical stimulus. Bend-sensitive neurons, in general, responded phaso-tonically and carried information on the direction and region of bending. This is the first experimental demonstration of bend sensitivity for arthropod setae. Cuspidate setae contain highly sensitive mechanosensory neurons; however, due to the rigid nature of these setae, whether they were bend sensitive or displacement sensitive could not be determined, and they were thus called “tactile neurons.” Bend-sensitive neurons, but not displacement-sensitive neurons or tactile neurons, showed graded responses to changes in osmolarity. The osmosensitivity of these neurons could mediate behavioral responses to changes in the osmolarity of seawater or food.