Cephalopod Eyes and Light Sensing Skin

DWhatley

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Humans, Squid Evolved Same Eyes with Same Gene
Tue, 05/06/2014 - 12:00pm
The Conversation, Malcolm Campbell



Complex beauty. Image: pacificklaus, CC BY-NC


Eyes and wings are among the most stunning innovations evolution has created. Remarkably these features have evolved multiple times in different lineages of animals. For instance, the avian ancestors of birds and the mammalian ancestors of bats both evolved wings independently, in an example of convergent evolution. The same happened for the eyes of squid and humans. Exactly how such convergent evolution arises is not always clear.
In a new study, published in Nature Scientific Reports, researchers have found that, despite belonging to completely different lineages, humans and squid evolved through tweaks to the same gene.
Eyes are the prize
Like all organs, the eye is the product of many genes working together. The majority of those genes provide information about how to make part of the eye. For example, one gene provides information to construct a light-sensitive pigment. Another gene provides information to make a lens.
Most of the genes involved in making the eye read like a parts list – this gene makes this, and that gene makes that. But some genes orchestrate the construction of the eye. Rather than providing instructions to make an eye part, these genes provide information about where and when parts need to be constructed and assembled. In keeping with their role in controlling the process of eye formation, these genes are called “master control genes.”
The most important of master control genes implicated in making eyes is called Pax6. The ancestral Pax6 gene probably orchestrated the formation of a very simple eye – merely a collection of light-sensing cells working together to inform a primitive organism of when it was out in the open versus in the dark, or in the shade.
Today the legacy of that early Pax6 gene lives on in an incredible diversity of organisms, from birds and bees, to shellfish and whales, from squid to you and me. This means the Pax6 gene predates the evolutionary diversification of these lineages – during the Cambrian period, some 500m years ago.
The Pax6 gene now directs the formation of an amazing diversity of eye types. Beyond the simple eye, it is responsible for insects' compound eye, which uses a group of many light-sensing parts to construct a full image. It is also responsible for the type of eye we share with our vertebrate kin: camera eye, an enclosed structure with its iris and lens, liquid interior and image-sensing retina.
In order to create such an elaborate structure, the activities Pax6 controlled became more complex. To accommodate this, evolution increased the number of instructions that arose from a single Pax6 gene.
Making the cut
Like all genes, the Pax6 gene is an instruction written in DNA code. In order for the code to work, the DNA needs to be read and then copied into a different kind of code. The other code is called RNA.
RNA code is interesting in that it can be edited. One kind of editing, called splicing, removes a piece from the middle of the code, and stitches the two ends together. The marvel of splicing is that it can be used to produce two different kinds of instructions from the same piece of RNA code. RNA made from the Pax6 can be spliced in just such a manner. As a consequence, two different kinds of instructions can be generated from the same Pax6 RNA.
In the new study, Atsushi Ogura at the Nagahama Institute of Bio-Science and Technology and colleagues found that Pax6 RNA splicing has been used to create a camera eye in a surprising lineage. It occurs in the lineage that includes squid, cuttlefish and octopus – the cephalopods.
Cephalopods have a camera eye with the same features as the vertebrate camera eye. Importantly, the cephalopod camera eye arose completely independently from ours. The last common ancestor of cephalopods and vertebrates existed more than 500m years ago.
Pax6 RNA splicing in cepahlopods is a wonderful demonstration of how evolution fashions equivalent solutions via entirely different routes. Using analogous structures, evolution can provide remarkable innovations
 

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Introduction to: Cephalopod Vision
Dr. James Wood and Kelsie Jackson (pdf)

Cephalopods are known to have excellent senses and of these senses, their vision is perhaps the best studied. At a first glance cephalopod eyes look very similar to those of humans, whales and fishes. With the exception of the externally shelled and primitive nautilus, all cephalopods can perceive focused images, just like we can. ...
 

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Marine Life Series: Octopus Eyes
Mark H 2007

The octopus is an extraordinary animal in many ways, but the eyes of this creature are especially incredible. When you consider that they, and their relatives the squid and cuttlefish (collectively known as Cephalopods), are related to mollusks such as clams and snails, this structure is even more amazing.
 

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Comparisons of visual capabilities in modern cephalopods from shallow water to deep sea
Chung, Wen-sung 2014 PhD Thesis

Squid have undergone a series of evolutionary changes to form the hydrodynamic body, well-developed senses, and large brain lobes, rendering the most intelligent and fast invertebrate. Remarkably, squid possess large eyes to catch prey and avoid distant threats. Aside from renowned visual performance of squid in well-lit conditions, their large eyes are adaptive to increase light-gathering ability, resulting that squid are active at nighttime as well as in the sunless deep sea.

In an effort to better understand visual function of squid at different light environments, this study aimed using three methods to approach the goals, including interspecific anatomical comparisons of visual systems, behavioural observations, and functional assay of visual system. In Chapter 2, contrast-enhanced magnetic resonance imagery (MRI) was applied to investigate intact coleoids. A digitised neural atlas has been initiated, provided a non-invasive method to identify internal structures. Given MRI anatomical inspections combined with histology, the post-reconstruction of three dimensional brain and eye anatomical models revealed several new morphological adaptations across diverse species, including fovea, retinal ridge, and retinal bump. Also, volume estimation using MRI improved the resolution of standard histological methods. Regional specialisations of the retina, changes of eye shapes, and optical lobe sizes were assessed. In addition to several novel findings, supported by methods in other chapters, these anatomical adaptations correlate well with the living strategy and the light condition of individual species. The retinal deformation and the resulting advantage of eyesight become a unique solution in their daily visual tasks.

Along with gross morphological changes in squid eye dimensions and the deformation of retinal layers, Chapter 3 and 4 focused on the retinal architecture and corresponding functional adaptations. Firstly, light-filtering mechanisms, pupillary activities and dynamic screening pigment movements, were well tuned to optimise light gathering abilities. Furthermore, optical properties of squid eye showed that the enlarged lens and its high resolving power are most likely adapted to enhance light capture and extend its visual range in the twilight realm instead of high resolution visual tasks. Furthermore, a new type of the retinal cell was discovered in the proximal region of the inner segment layer in a group of mid-water squid. The depth distribution range of these squid possessing this dual layered retina was usually broader (50-1000 m) than the depth range (50-400 m) of those contained a regular retina. Positive immuno-histological labelling in this new form of the 2nd order retinal cells showed cross connections between cells in the retina, indicating that squid are likely to develop a neural summation mechanism to enhance light sensitivity analogous to the ganglion cells for deep-sea fish. This type of cross-connectivity in cephalopods has not been noted previously.

The second part of this study aimed to explore the visual function in situ and ex vivo using a common reef squid, Sepioteuthis lessoniana. The assumption that a single class of photoreceptor in cephalopod has a single type of visual pigment has been accepted in the literature with an exception of a Japanese firefly squid, Watasenia scintillans, which three different visual pigments are embedded in three receptors with different morphological features. According to morphological evidence in Chapter 2 and 3, S. lessoniana possesses a unique retina which comprises of two types of photoreceptors with different arrangements of rhabdomere, similar to the photoreceptors of the banked retina of W. scintillans. In Chapter 5, a new protocol of microspectrophotometry (MSP) was developed to solve the difficulty in bleaching visual pigment of cephalopod and accelerate the procedure in investigating the spectral absorption of visual pigment of squid. Furthermore, using this method enables to measure the spectral sensitivity of an individual photoreceptor rather than the regular measurement of the retinal extracts of an entire retina. Given these advantages, the distribution pattern of visual pigment across the retina in S. lessoniana was therefore reconstructed, representing small amounts of variance in spectral sensitivity. Although MSP results demonstrated that this common reef squid only contains a single visual pigment as do all other shallow water cephalopods known, this new method provides a new way in studying cephalopod visual pigment in the future study.

In Chapter 6, a new optical adaptation in squid is described. The eyes of less than terminal adult phases display a retinal bump within the eye, resulting in hyperoptic defocus in a large portion of the dorso-temporal retina. This has been confirmed in S. lessoniana in vivo and vitro. Although this blurring of vision in the critical region of the eye coordinating tentacular strike seems disastrous for these visually-guided predators, the deformation of retina combined with a unique head bobbing behaviour becomes an efficient solution to estimate the distance of objects. When head bobbing, the image of interest objects consecutively pass from focused and defocused retinal regions and the resulting focus differential provides squid a simple cue for distance without stereopsis or parallax, prior to rapid prey-catching tentacular strikes. This unique range finding mechanism is an adaptation to hunting, defense and other important object size identification tasks, against a contrast-poor background.

The third part of this study was using new design baited deep-sea cameras with illumination which is invisible to the animal, allowing the observation of squid visual behaviours in their natural habitat between 500-1100 m. In Chapter 7, the visual ecology of deep-sea squid in areas of diminishing sun light and more frequent bioluminescent flashes was investigating using unobtrusive in situ videography. Custom-designed baited cameras with animal-invisible illumination recorded natural behaviours of squid from four different species at depths between 525-790 m. A light lure emitting artificial bioluminescent flashes triggered apparent squid foraging and attacking behaviours. These included the first observation of feeding behaviour of the giant squid, Architeuthis dux in its natural habitat. Aside from the light lure to attract attention, the use of bait at different ambient light conditions demonstrated that decreasing ambient light intensity significantly disrupted the successful feeding rate in the Humboldt squid, Dosidicus gigas.

Overall, this study provides several new insights into anatomical adaptations of retina and brain in several cephalopod species as well as corresponding functional improvements which are associated with optimising visual capabilities in a large depth and illumination range. In conclusion, cephalopod vision and visual behaviour appear more complex rather than our previous expectation.
Abstract contains an explanation of bobbing behavior and eye blurring to clearly locate an object.
 

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Some Evidence for Colour-Blindness in Octopus
BY J. B. MESSENGER, A. P. WILSON AND A. HEDGE 1973 (full pdf)

INTRODUCTION In this paper we put forward evidence from two kinds of experiments that suggests very strongly that octopuses are colour-blind. Colour-vision in cephalopods has received intermittent attention in the last fifty years, and, using different genera and different experimental techniques, several workers have arrived at different conclusions; their results are summarized in Table 1. With the exception of Orlov and Byzov, and of Hamasaki, all the authors are guilty of one or more of three serious errors: failure to take into account the spectral sensitivity curve of the subject, failure to control for the difference in brightness between test objects, and, in the behavioural experiments, inadequate quantification of results, which are presented without conventional statistical analysis. All this earlier evidence, therefore, is suspect. In 1961, in a paper that seems to have been overlooked, Orlov and Byzov reported an electrophysiological investigation of the isolated cephalopod retina and found evidence that a given ERG can be produced by light of different wavelengths if compensations for brightness differences are made; and by using the method of colorimetric substitution they were able to change from one illuminating wavelength to another without affecting the ERG. They did not find a Purkinje shift. This was apparently true for a squid, Ommastrephes sloanei-pacificus, as well as for the large Pacific octopus, Octopus dofleini (Orlov & Byzov, 1961, 1962). Later Hamasaki (1968 a, b) examined intact O. briareus and O. vulgaris and found that the darkadaptation curve was monotonic, with no evidence of the discontinuity normally associated with a dual retinal system; again there was no evidence of a Purkinje shift, suggesting there is only one receptor system in the octopus retina. Meanwhile Hubbard and her collaborators (Hubbard & St George, 1958; Brown & Brown, 1958; Kropf, Brown & Hubbard, 1959) had characterized a photopigment, rhodopsin, in several cephalopods; for O. vulgaris rhodopsin see Fig. 1. Then, in 1965, Hara and Hara found a second pigment in the cephalopod retina - retinochrome, whose peak absorption (490 run in O. vulgaris) was close to that of rhodopsin (see also Hara & Hara, 1967; Hara, Hara & Takeuchi, 1967). It is not clear whether this pigment occurs in the receptors, however (see Discussion). Morphologically Young (1962 a) had already recognized several different types of retinal cell in Octopus, while Hagins (1965) distinguished two types in the squid retina. Taken together these findings suggest that the cephalopod retina could possess a system for detecting wavelength. Now octopuses are excellent subjects for learning experiments ...
 

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Sensitivity to Blue light and using blue moonlights instead of red. This is a paper written under Doctor Hanlon that shows the biological reasons for S. Officinalis being sensitive to blue light. It is significant to ceph keepers as it is often mentioned but difficult to find scientific studies.

The paragraph that suggests blue sensitivity:

Both lens and cornea showed high transmittance in the 470- 550 nm range, to which cuttlefish are most sensitive (Fig. 1A). The lens was found to be somewhat less transparent in the long wavelengths (>590 nm), and both lens and cornea absorbed short-wavelength radiation, acting together as a long pass filter with 50% transmission at about 370 nm
Here is a color chart that shows the color bands in these wave lengths. In brief Blue->Cyan-Green:440-565 (590 = yellow)
Unfortunately, the study was intended to find the short wave length limits and the longer, red colors were not included in the experiment (oddly this paper was referenced as the source of cephalopods not seeing red but is not part of the paper at all)

UV Radiation Blocking Compounds in the Eye of the Cuttlefish Sepia officinalis
Nadav Shashar, Ferenc I. Hdrosi, Anastazia T. Banaszak’, and Roger T. Hanlon (Marine Biological Laboratory, Woods Hole, Massachusetts 02543)

A 1968 research paper by D.I. Hamasaki, The era-determination spectral sensitivity of the Octopus, should identify the red spectrum blindness but I have not been able to locate even the abstract.
 
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Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides M. Desmond Ramirez, Todd H. Oakley 2015 (See this thread to obtain a copy of the paper)

We know that octopuses accept red light as no or very little light and there have been indications that blue light may be brighter to them than white light, suggesting using a blue moon light is not a good idea for night viewing. The recent study showing the skin itself is light sensitive and uses the same light sensing proteins found in the eyes. The study shows that there is no chromatophore expansion with red light, notable expansion with white light and the greatest expansion with blue light supporting the current thinking about light sensitivity.

ABSTRACT
Cephalopods are renowned for changing the color and pattern of their skin for both camouflage and communication. Yet, we do not fully understand how cephalopods control the pigmented chromatophore organs in their skin and change their body pattern. Although these changes primarily rely on eyesight, we found that light causes chromatophores to expand in excised pieces ofOctopus bimaculoides skin. We call this behavior light-activated chromatophore expansion (or LACE). To uncover how octopus skin senses light, we used antibodies against r-opsin phototransduction proteins to identify sensory neurons that express r-opsin in the skin. We hypothesized that octopus LACE relies on the same r-opsin phototransduction cascade found in octopus eyes. By creating an action spectrum for the latency to LACE, we found that LACE occurred most quickly in response to blue light. We fit our action spectrum data to a standard opsin curve template and estimated the λmax of LACE to be 480 nm. Consistent with our hypothesis, the maximum sensitivity of the light sensors underlying LACE closely matches the known spectral sensitivity of opsin from octopus eyes. LACE in isolated preparations suggests that octopus skin is intrinsically light sensitive and that this dispersed light sense might contribute to their unique and novel patterning abilities. Finally, our data suggest that a common molecular mechanism for light detection in eyes may have been co-opted for light sensing in octopus skin and then used for LACE.
 

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On the three visual pigments in the retina of the firefly squid, Watasenia scintillans
Masatsugu Seidou, Michio Sugahara, Hisatoshi Uchiyama, Kenji Hiraki, Toshiaki Hamanaka,Masanao Michinomae, Kazuo Yoshihara, Yuji Kito 2015 (subscription)

Summary
The deep-sea bioluminescent squid, Watasenia scintillans, has three visual pigments: The major one (A1 pigment) is based on retinal and has λ max = 484 nm, the second one (A2 pigment) is based on 3-dehydroretinal and has λ max = 500 nm, and the third one (A4 pigment) is based on 4-hydroxyretinal and has λ max = 470 nm. The distribution of these 3 visual pigments in the retina was studied by HPLC analysis of the retinals in retina slices obtained by microdissection. It was found that A1 pigment was not located in the specific region of the ventral retina receiving the down-welling light which contains very long photoreceptor cells, forming two strata. A2 and A4 pigment were found exclusively in the proximal pinkish stratum and in the distal yellowish stratum. The role of these pigments in the retina is hypothesized to involve spectral discrimination. The extraction and analysis of retinoids to determine the origin of 3-dehydroretinal and 4-hydroxyretinal in the mature squid showed only a trace amount of 4-hydroxyretinol in the eggs. Similar analysis of other cephalopods collected near Japan showed the absence of A2 or A4 pigment in their eyes
 

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An unexpected diversity of photoreceptor classes in the Longfin squid, Doryteuthis pealeii
Kingston, Alexandra C. N., Wardill, Trevor J.,Hanlon, Roger T.,Cronin, Thomas W. 2015 (Woods Hole Open Access Server)

Cephalopods are famous for their ability to change color and pattern rapidly for signaling and camouflage. They have keen eyes and remarkable vision, made possible by photoreceptors in their retinas. External to the eyes, photoreceptors also exist in parolfactory vesicles and some light organs, where they function using a rhodopsin protein that is identical to that expr essed in the retina. Furthermore, dermal chromatophore organs contain rhodopsin and other components of phototransduction (including retinochrome, a photoisomerase first found in the retina), suggesting that they are photoreceptive. In this study, we used a modified whole - mount immunohistochemical technique to explore rhodopsin and retinochrome expression in a number of tissues and organs in the longfin squid, Doryteuthis pealeii. We found that fin central muscles, hair cells (epithelial primary sensory neu rons), arm axial ganglia, and sucker peduncle nerves all express rhodopsin and retinochrome proteins. Our findings indicate that these animals possess an unexpected diversity of extraocular photoreceptors and suggest that extraocular photoreception using v isual opsins and visual phototransduction machinery is far more widespread throughout cephalopod tissues than previously recognized.
Description
Data are arranged into 12 Zip files, one for each figure (Figures 1 - 6) and one for each supporting figure (S1 - 6). Each Zip file includes the original images used for figures and supporting figures. Scale bars in all figures and supporting figures are 25μ
 

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Why octopuses? Have we learned anything from studying their brains?
J. B. Messenger
Science Progress (1933-)
Vol. 72, No. 3 (287) (1988), pp. 297-320

Older (1988) article that can be fully accessed by registering for a free account. linking here because of the interesting section on octopus sight, noting that they cannot distinguish between a right and skewed figure.
 

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