Figure 2: Dolichpteryx longipes, a fish with a conventional tubular eye with refractive optics, and a diverticulum based on reflecting optics. A Dorsal view of a living specimen; the dotted line indicates the plane of sectioning of the following micrographs. B Thin section of the tubular eye and the diverticulum stained with methylene blue. C Diagram of the adjacent section: sclera-blue; choroid-black; retinal pigment epithelium-brown; rod inner and outer segments-green; remaining retinal layers-yellow; mirror-grey. D Visual field angles of the tubular and the diverticular eye. E & F Bright field and dark field micrograph of the diverticulum: Note the bright reflection of the mirror in dark field illumination with polarised light. G Schematic representation of ray tracing modelling demonstrating the function of the focussing mirror of the diverticulum( Fresnel principle) H & I High magnification bright field and dark field light micrographs of the mirror structure showing reflective crystals. J Electron micrograph of stacks of guanine crystals showing alternation of crystals and cytoplasm, each layer about 120nm wide, corresponding to the quarter wavelength of the incoming light and resulting in mirror-like reflection.
of alternating layers( bioluminescence: 480 nm) of different optical densities is well known from other animals to act as a potent reflective device. In addition, we recorded the orientations of these crystals along the length of the mirror and observed that they started almost parallel to the septum ventrally, and then increasingly changed the orientation more dorsally. Modelling these data demonstrated that the incoming light from below was thus effectively reflected and focussed at the outer limiting membrane level, i. e. the rod outer segment acceptance opening of the lateral retina( Fig 2G). By adding such a downward-facing diverticulum to its tubular eye, therefore, Dolichopteryx almost doubles the range of its visual field( Fig 2D) and is capable of surveying the waters above and below.
We have been privileged to be the first to report this mirror-based focussing device in the diverticulum of the Dolichopteryxeye, an optical arrangement already known from several arthropods and described by K. Kirschfeld, one of the founders of the Tübingen Graduate Training Centre and IMPRS for Neuroscience, but never before observed in vertebrates. Interestingly, focussing lenses with a similar optical principle were developed by A. J. Fresnel in the 19th century for early lighthouses.
As exciting as our discovery of the Dolichopteryx mirror eye was at the time, it turned out to be the key to another surprising story when we looked at the eyes of the other members of the barreleye family. The opisthoproctids comprise seven genera and 19 species; however, the taxonomic relationships are far from settled. All of these have tubular eyes with diverticula of various sizes and degrees of complexities. Two families Opisthoproctus( Fig. 1) and Winteria have tiny outpocketings made up of all three ocular layers, i. e. sclera, choroid and retina, with an unpigmented ventrolateral“ window” admitting light to a diverticular retina that lacks ordered, mirror-like crystals.
The intriguing observation here is that in larval specimens of Dolichopteryx, described earlier, the diverticulum looks very similar to this simple, or“ primitive” situation in Opisthoprocus. It is tempting to speculate that this might be another case where ontogeny recapitulates phylogeny. A further barreleye species( Bathylychnops) has a diverticulum considerably larger than in the two previous families; however, instead of a crystal mirror it uses a corneal( connective tissue) lens to focus light onto the retina of the diverticulum. Finally, Rhynchohyalus presents a situation at first sight very similar to the“ mirror eye” diverticulum of Dolichopteryx. However, the mirror with its guanine crystals, which in Dolichopteryx is derived from the retinal pigment epithelium, in Rhynchohyalus is made up by iridocytes of the choroid.
These observations lead to at least two further questions:( i) What is so special about barreleyes that makes them the only family of deep-sea fish( known to date) to have evolved such a variety of different eye designs? And( ii) What are the taxonomic relationships within the opisthoproctid family?
Clearly more morphological data will not help; instead, molecular data and markers are needed to solve these questions. And since these require fresh tissue for DNA or RNA analysis, more deep-sea cruises are planned. Apart from the excitement of exploring the fascinating fauna of the deep, the work on a research ship provides an unforgettable social experience: a combination of hard work on board, focussed and without the distractions of the lab at home, coupled with intense and productive interaction with friends and colleagues.
Prof. Dr. Hans-Joachim Wagner works at the University of Tübingen in the Department of Anatomy and enjoys mixing both scientific discovery and thrill-seeking adventure.
[ 1 ] Wagner, H.-J., Douglas, R. H., Frank, T. M., Roberts, N. W. & Partridge, J. C.( 2009). A novel vertebrate eye using both refractive and reflective optics. Current Biology, 19, 106-114
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