Clinical and Experimental Ophthalmology

2004;

32

: 559–560

Editorial

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Editorial

An enigmatic eye: what can we learn?

It is unlikely that Charles Darwin ever saw a living tuatara,but he may have seen museum specimens of this pivotalcreature. A contemporary of Darwin, Dr Albert Gunther, atthe British Museum in 1867, recognized that the Tuatarawas not another iguanid or agamid, but belonged to anorder,

Rhynochocephalia

, thought to be long extinct. How-ever, Darwin would have understood the importance of thetuatara as a relict capable of teaching us about evolution ina different period.

The tuatara or its immediate ancestor probably evolvedin the early Jurassic period, approximately 140–200 millionyears ago, and has changed little since. The creature repre-sents a phylogenetic window into the predecessors of thedinosaurs, other reptiles, birds and even mammals. As hasbeen well known since Spencer,

1

the tuatara, as some otherreptiles, has a median third eye on the dorsal aspect of itsskull. This third eye, then, provides us with an image ofevolution’s attempts at photoreception in the early Jurassic.

The article of Ung and Molteno in this issue

2

providesfurther investigation into the third eye of the tuatara withexcellent histology and speculation as to function. Althoughthe reptilian pineal complex is probably responsible forthermoregulation and the animal’s circadian rhythm, thisorgan may be responsible for much more.

A remnant of the reptilian pineal complex, the pinealbody in other vertebrate species is known to secrete ayellow-orange pigment, pinopsin.

3

This novel photo-pigment is similar to rhodopsin although its functionremains unclear. In another example of the obscure nature ofthis organ, the pineal body has an autoantigen, retinal-Santigen, documented to participate in both autoimmuneuveitis and ‘pinealitis’ in rats.

4

In humans, what remains of the third eye is the pinealgland, and it has been well studied although its function(s)remains murky. It is known that the human pineal gland, asin reptiles, secretes melatonin among other neuroendocrinesecretions that participate in the hormonal regulation of manyother organs, and even participates in immuno-modulation.

5

In humans, this obscure organ has also been shown to bethe site of the neuroblastoma found in the trilateral retino-blastoma syndrome, suggesting that the primitive photo-receptor elements may still be present at least in terms of thepotential for malignancy.

6

There may be more to be learned from this obscureorgan, or it may be an evolutionary dead end as it seems tobe in decline. The organ is found only in some reptiles andprobably reached its zenith in those orders of reptiles whereit exists. Birds and mammals have a remnant, as mentioned,

but do not have the same complexity in the organ as is foundin reptiles. Even in reptiles the third eye is incompletelyformed, although there is a high degree of variability.

For example, as noted in the article by Ung and Mol-teno,

2

the photoreceptors are not inverted as are those ofthe lateral eyes. Why should the photoreceptors be evertedin the third eye but not in the lateral eyes? As explained byEakin in

The Third Eye

,

7

it all relates to embryology. Invertebrates, eyes begin as evaginations of the diencephalonto create optic vesicles, and the lateral eyes proceed toinvaginate forming optic cups. However, in the tuatara aswell as other reptiles, the third eye does not invaginate.Furthermore, it is lined with cilated epithelia that wouldotherwise become the photoreceptors with the cilatedportion of the cells extending inward toward the centre ofthe vesicle. The most distal or most dorsal portion of thevesicle that would become the third eye condenses into alens. This creates a cyst lined with ciliated cells essentiallydirected towards the interior of the cyst, and thus evertedinstead of inverted as those of the lateral eyes. The cells thatcondense into a lens, then, are homologous to cells thatwould become retinal cells in the lateral eye. Interestingly,the remaining cilated cells that line the vesicle will differen-tiate into pigment epithelium as well as photoreceptors, andthe pigment epithelium will be distal to the photoreceptors.A complete ‘normal’ vertebrate eye never forms as the thirdeye, as if missing an embryological stimulus.

Hence, the pineal complex may be an abandoned evolu-tionary cul-de-sac that does not provide enough of a benefitto be worth its phylogenetic continuation. Nevertheless,from a human standpoint, and especially from an ophthal-mic standpoint, the pineal body seems to have enough cluesassisting in the understanding of the eye and visual process-ing to deserve our attention to its evolution.

Ivan R Schwab

MD

1

and G Richard O’Connor

MD

2

1

Professor of Ophthalmology, University of California, Davis, and

2

Professor Emeritus of Ophthalmology, University of California,San Francisco, CA, USA

R

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Hatteria

.

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4. Donoso LA, Merryman CF, Sery TW

et al.

S-antigen: charac-terization of a pathogenic epitope which mediates experi-mental autoimmune uveitis and pinealitis in Lewis rats.

Curr EyeRes

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: 1151–9.5. Guerreor JM, Reiter RJ. Melatonin–immune system relation-

ships.

Curr Topics Med Chem

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6. Kivela T. Trilateral retinoblastoma. A meta analysis of heredi-tary retinoblastoma associated with primary ectopic intra-cranial retinoblastoma.

J Clin Oncol

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: 1829–37.7. Eakin RM.

The Third Eye

. Berkeley: University of CaliforniaPress, 1973.