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Things are looking up

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The barreleye (Macropinna microstoma) is a member of the Opisthoproctidae family, a bizarre collection of approximately 11 oceanic species, all of which are mesopelagic to bathypelagic in habit with no shortage of unusual ocular adaptations evolved to master this biologically forbidding environment.

M microstoma is an odd, translucent (even its brain is visible), little fish with a maximum length of about 5 cm (specimen illustrated on the cover measured 4.4 cm). Living at depths up to 900 metres below sea level, where darkness, extreme pressure, and numbing cold will winnow the weak, this solitary fish faces challenges that evolution has met with creative, but not entirely surprising, innovations. This particular species has very large spherical pigmented crystalline lenses, and vertically directed tubular eyes among other adaptations.

Lens pigmentation may occur in diurnal vertebrates and in these species the pigment is a soluble component of the lens cells and is freely diffusible throughout the cells within the crystalline lens. This yellow pigmentation, seen in mammals such as the ground squirrel (Spermophilus beecheyi), is an adaptation believed to improve acuity by reducing chromatic aberration of the shorter wavelengths.

Lens pigmentation may also occur as an age related phenomenon (as cataract surgeons know well). This pigmentation is probably a degenerative ageing change and a result of ultraviolet exposure. But, some ageing changes in pigmentation of the crystalline lens are not degenerative. Some mesopelagic fish (Argyropelecus affinis hatchetfish in the family Sternoptychidae) have an abrupt pigmentation of the lens fibres beginning at approximately the mid-point in their maturation cycle, and the pigment is found only in the lens cells produced from that point forward in its development. Hence, in these fish, only the more peripheral lens cells accumulate pigment, and not the nucleus, which remains clear throughout life. These carotenoid-like pigments are associated with the crystallins of the lens fibres and are not diffusible between cells.

The lens pigmentation of M microstoma is unlike that of any of the other known species and probably represents a peculiar form of convergent evolution because it seems that lens pigmentation has evolved several times and for different reasons. Furthermore, lens pigmentation is uncommon in mesopelagic or bathypelagic species.

Although the pigment is freely diffusible throughout the crystalline lens of M microstoma, it is a distinctly different pigment with different spectral qualities from that found in terrestrial vertebrates or in other fish, at least those that have been studied (McFall-Ngai MM, Biol Bull1988;175:397–402). And why would any animal want a pigmented lens, since any pigmentation will, at least to some extent, limit photon capture and be an impediment at this depth.

The yellow lens pigmentation probably has several functions. These lenses would filter out at least a portion of the downwelling light especially on the shorter end of the wavelength spectrum and act as a transmission filter removing wavelengths shorter than perhaps 450 or 460 nm. This would increase acuity by decreasing chromatic aberration, limiting short wavelength light scatter within the eye, and probably by increasing contrast sensitivity by eliminating the “blue haze.” This might be of service to epipelagic fish, but wavelengths longer than 450 nm never reach the eye at these depths, having been filtered out by the water column, so such pigmentation would probably offer only a slight advantage. But, does this convey a significant enough evolutionary advantage to sacrifice bandwidth and photon capture?

There is at least one additional possibility. In a well considered manuscript, Muntz offers evidence for an interesting and very clever alternative. Many mesopelagic prey (and sometimes predator) species have photophores or bioluminescent organs on their ventral surface. These organs generally produce light at approximately 475 nm which is exactly the peak wavelength of the downwelling light from the surface. Hence, any prey species with photophores producing this wavelength would have almost perfect camouflage and not provide a silhouette that would betray its presence and path. But, Muntz predicts that this camouflage will not be effective against a predator that has a high pass lens filter in the form of a yellow lens because this filter will make the bioluminescent photophores (or other forms of bioluminescence) appear brighter since downwelling light and bioluminescent light are not identical. Bioluminescence often has a broader spectral composition than the background or downwelling light. Furthermore, if the photoreceptor visual pigment is tuned to a wavelength such 480 nm or longer (and generally fish at this depth do have such visual pigments), this bioluminescent target will be even brighter and more visible over a greater distance. Muntz also suggests that such predators must be looking upward to maximise such benefit (Muntz WRA, J Mar Biol Ass UK1976; 56:963–76). If this species has two visual pigments and does not live in a monochromatic world, these pigmented lenses would be of increased service by allowing the fish to distinguish the wavelength and intensity of a bioluminescent signal.  M microstoma, as you can see from the photograph, is looking straight up with very large eyes and yellow lenses, but its visual pigments have not been studied. Bioluminescence is common among the smaller invertebrates that are part ofM microstoma's diet. Perhaps breaking the camouflage of these invertebrates is important to limit the search in time and space for food to maximise capture in such dim and hostile environment, since meals may be not be abundant.  The crystalline lens in this species is interesting for other reasons, and should be considered further. This species, as with its close relatives in the same family, approach what is called the evolutionary “quit” point for vision. Below about 1000 metres there is no downwelling light, even in the clearest of ocean waters. So, at these depths, some fish (and invertebrates) have begun using bioluminescence to communicate and even to illuminate much like a torch. Nevertheless, the evolutionary pressures must respond to the lower light levels by making every photon count. Hence, in mesopelagic and bathypelagic fish the pupil is fixed and dilated and there is no pupillary constriction. The lens is very large and almost perfectly spherical (as it is in most fish), and the pupillary aperture matches the equatorial diameter thus using the entire lens for photon capture. This would leave the eye susceptible to spherical and chromatic aberration especially from the more peripheral portions of the lens, creating a blurred image. To solve this problem, evolution has found an interesting solution. Most fish lenses have a higher index of refraction at the centre of the lens and a progressively decreasing gradient from the centre to the periphery eliminating chromatic aberration for all practical purposes (Fernald RD, Wright SE,Nature1983;301:618–20).

Since the eyes look upward and the lens protrudes through the pupil even to the point of affecting the contour of the dorsal surface, the visual field could be predicted to be almost hemispherical. This tubular eye does have photoreceptors rising on the sides of the “tube” to a point nearly equivalent to the equator of the lens thus assuring the sensitivity of that hemispherical field even if the far peripheral portions of the retina would be too close to the lens to be in proper focus. Nevertheless, this portion of the retina could sense movement of any bioluminescent object.

So, for this translucent bottom dweller with relatively enormous eyes and several adaptations to maximise photon capture, prey recognition, and perhaps protection against predators, things are definitely looking up.—Ivan R Schwab, MD, UC Davis Department of Ophthalmology, 4860 Y Street, Ste 2400, Sacramento, CA 95817, USA (irschwab{at}ucdavis.edu)

Thanks to Cynthia Klepadlo and the Scripps Institution of Oceanography for the specimen (SIO71-65).

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