Eye development in southern calamry, Sepioteuthis australis, embryos and hatchlings

Introduction

The cephalopod eye, infamous for its convergent evolution with the vertebrate eye, is crucial to the success of all cephalopods.  Specifically, coleoid cephalopods (octopus, squid, and cuttlefish) are ideal model organisms for comparison to the human eye.  The nearly spherical coleoid eye consists of many of the same elements as the human eye—the iris, lens, pupil, and retina composed of photoreceptor cells (Fig. 1) (McCormick and Cohen 2012).

Figure 1. Coleoid cephalopods are often used as model organisms to the the similarity in eye structure to the human eye. http://cephalove.blogspot.com/2010/05/octopus-visual-system.html

Unlike the human eye, the coleoid eye focuses and tracks images through movement of the eye (like a camera) rather than changing the shape or curvature of the lens (Yoshida and Ogura 2011).  This movement produces a perfectly focused and very sharp image on the retina (Bozzano et al. 2009).  Additionally, the coleoid eye can detect polarized light, which allows these organisms to see in both photic and scotopic conditions (Bozzano et al. 2009, Talbot and Marshall 2010, Talbot and Marshall 2011).  The ability to see and track prey in these different light conditions has allowed these cephalopods to become dominant and often top predators throughout many marine environments (Bozzano et al. 2009, Talbot and Marshall 2010).

Mechanism for Adapting to Variable Light Conditions

To adapt to variable light conditions, adult coleoid cephalopods use two different mechanisms—mobile pupil aperture and photoreceptor morphology (Bozzano et al. 2009, Talbot and Marshall 2011, McCormick and Cohen 2012).  The pupil constricts based on the ambient light level to control the amount of light entering the eye and to centralize it to the retina (Bozzano et al. 2009, Talbot and Marshall 2010, McCormick and Cohen 2012).  This function enables the cephalopod to focus rapidly under changing light conditions (McCormick and Cohen 2012).  Additionally, it allows these cephalopods to focus on a single area in the line of vision, which better enables them to track prey (McCormick and Cohen 2012).  The actual ability to detect and respond to the polarized light in the environment depends on the arrangement of the photoreceptors (Talbot and Marshall 2011).  The rapid detection is based on the pupil aperture directing light to specific photoreceptors, which work to screen pigment migration together while enlarging and contracting (Bozzano et al. 2009, Talbot and Marshall 2011).

Figure 2. A picture of the model squid, Sepioteuthis australis. http://www.ryanphotographic.com/squid.htm

These mechanisms that allow the eye to detect polarized light are very well understood in the adult coleoid cephalopod, but they have yet to be explored in embryo and hatchling cephalopods.  The study by Bozzano et al. explores the morphological development of the visual system in southern calamary, Sepioteuthis australis (Fig. 2), and aims to determine if the photomechanical mechanisms utilized in adult cephalopods are present at or before hatching.

Eye Development

Bozzano et al. tracked the development of the eye in southern calamary embryos and hatchlings.  To do this they identified the developmental stage of embryos using the scale of Arnold, which ranges from 1-30 (30 being a hatchling) and used light imaging techniques to visually record the progress of the eye.  The embryos were observed for the full length of time, but histology was only carried out starting at stage 18.

They found the eye primordium was first visible at stage 16 and by stage 20 the lens primordium was clearly visible (Figure 3A). By stage 24, the optic vesicle was hemispheric with more defined lentigenic cells, and pigment became visible in the iris (Fig. 3B and 3C).  Additionally, some cells were observed to differentiate into photoreceptor proximal and photoreceptor distal processes.  At stage 26, the eye was fully pigmented, the cornea became visible, and the anterior and posterior lens segments were clearly formed (Fig. 3D).  The optical vesicle showed differentiation of the neural retina at stages 28 and 29.  This differentiation clearly separated the photoreceptor nuclei and support cell nuclei through a basement membrane.  At this point, a near spherical lens mass formed the inner and outer lens and the cornea fully enclosed the eye (Fig 3E).

Figure 3. Embryonic development of the squid eye. Images from stages 20-29 show the progression of the eye throughout embryonic development. A) Stage 20. Lens is clearly visible. B) Stage 24. Embryo with yolk sac and chorion. C) Magnified eye from stage 24. Pigment visible in darker iris. D) Stage 26. Fully pigmented eye. E) Stage 29. Cornea fully encloses the eye. F) Magnified stage 29. The pupil is almost closed. http://eprints.jcu.edu.au/7957/

Photomechanical Responses
Bozzano et al. examined pupil response and visual pigment migration in light- and dark-adapted individuals.  They looked at individual responses to these light conditions at the end of embryonic development (stage 28), hatchlings (stage 30), and 2 days post-hatching.  Images of the eyes were used to measure pupil aperture areas.  Visual pigment migration was measured using the length of the photoreceptor distal processes and the distance of pigment migration along the length of the photoreceptor in different areas of the retina (dorsal, central, ventral, anterior, and posterior sectors).  The percentage of pigment migration index, pmi, was then calculated by dividing the pigment migration by the length of the distal process.  A pmi of 100% represents pigment that completely covers the full length of the photoreceptors.

Figure 4. Pupil aperture variation in light- and dark-adapted individuals. A) Stage 28 embryo shows fairly circular aperture in the dark. B) Stage 28 embryo shows reduced aperture after being exposed to light. C) 2 days post hatchling (dph), pupil aperture is still circular in the dark. D) 2 dph pupil aperture is reduced and E) almost completely closes in some 2dph individuals. http://eprints.jcu.edu.au/7957/

At stage 28, the pupils were relatively spherical in shape under dark conditions whereas the pupil was partially occluded by the iris diaphragm when illuminated (Fig. 4A and Fig. 4B, respectively).   In the dark, the pmi ranged from 68.4% to 100% depending on the area of the retina in question.  In the light, most retinal regions had 100% pmi, meaning their rhabdomes were fully screened by pigment.

In the hatchling stage, a withdrawal of pigment was observed in all retinal regions except the ventral anterior part under dark conditions.  The pupil dilation was not reported for the dark conditions.  In the light conditions, pupil area was reduced by one-third to one-half of its full aperture.  The pigment was reported to almost completely screen all retinal regions except in the dorsal posterior.

Finally, in the 2 days post-hatching calamary, the pupils were observed to be almost completely spherical (Fig. 4C).  This contrasts sharply from the pupil exposed to light conditions, which was observed to be partially or completely occluded (Fig. 4D/E).  The pigment was reported to be 100% under both light and dark conditions.

Discussion

Tracking the progression of the coleoid eye throughout embryonic development revealed that the retina and lens were complete just prior to hatching.  Bozzano et al. suggest this is important because of the relationship between form and function.  The timing of development can impact visual capabilities after hatching giving the cephalopod an advantage over prey and its potential predators.  The results quantitatively show that pigment migration does occur before hatching in these cephalopods, as well.  This is of high importance because it means these cephalopods have already developed a photomechanical response before they hatch, which is not seen in other individuals until after metamorphosis.  This is advantageous because screening pigment migration appears to be related to enhanced image quality in retinal areas meaning this squid has a strong advantage over many of its less visually acute neighbors.

This paper’s strength lies in the fact that it is one of the first, if not the first, to track eyeball development throughout the embryo stages in a coleoid cephalopod.  It does a good job of providing a lot of strong evidence in determining the progression of the eye at different stages through use of high-resolution photos (see Fig. 3 and Fig. 4 above).   This study is weak in its experimental approach for determining pupil aperture.  It is limited to recording pupil aperture in dead squid for both light- and dark- adapted individuals.  Additionally, dark-adjusted squid must be transferred to light-filled environments for further analysis after death.  This has a high potential of affecting the pupil aperture meaning the data recorded are only crude estimates.

Despite this flaw, this experiment is very exciting because it shows the potential to understand eyeball development in all coleoid cephalopods.  This or a similar approach can be taken in an effort to better understand coleoid eye development in the embryo stages.  As we gain understanding in the development of the coleoid eyeball, we will hopefully gain understanding in the development of the human eyeball.  The potential results from these experiments are enormous because they could offer solutions to genetic sight disorders.

Citations

Bozzano, A., P. M. Pankhurst, N. A. Moltschaniwskyj, and R. Villanueva. 2009. Eye development in southern calamary, Sepioteuthis australis, embryos and hatchlings. Marine Biology 156:1359-1373.

McCormick, L. R. and J. H. Cohen. 2012. Pupil light reflex in the Atlantic brief squid, Lolliguncula brevis. The Journal of experimental biology 215:2677-2683.

Talbot, C. M. and J. Marshall. 2010. Polarization sensitivity and retinal topography of the striped pyjama squid (Sepioloidea lineolata – Quoy/Gaimard 1832). The Journal of experimental biology 213:3371-3377.

Talbot, C. M. and J. N. Marshall. 2011. The retinal topography of three species of coleoid cephalopod: significance for perception of polarized light. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 366:724-733.

Yoshida, M. and A. Ogura. 2011. Genetic mechanisms involved in the evolution of the cephalopod camera eye revealed by transcriptomic and developmental studies. BMC Evolutionary Biology 11:1-11.

1 Response to Eye development in southern calamry, Sepioteuthis australis, embryos and hatchlings

  1. Great article, only a lot of difficult term

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