Evolutionary attempts at 4 eyes in vertebrates

Ivan R. Schwab, Viet Ho, Alan Roth, Thomas N. Blankenship, Paul G FitzGerald, Robert D. Yee

Research output: Contribution to journalArticle

10 Scopus citations

Abstract

Purpose: To understand and compare the optical, histological, and ecological differences among 4 vertebrate species that have had evolutionary attempts toward 4 eyes. Methods: An evolutionary attempt at 4 eyes is defined as the duplication of one or more structures integral to the refraction or interpretation of the visible spectrum for that animal. We reviewed and compared the known optics, histology, and ecology of each of these vertebrate species with attempts at 4 eyes including Anableps anableps, Dialommus fuscus, Mnierpes macrocephalus, and Bathylychnops exilis. These animals have developed portions of ancillary eyes that have diverged from the primary globe in 3 different patterns. At least 1 specimen of each of these vertebrate species known to have 4 eyes was examined histologically and compared to the animal's ecology and current cladistic relationship. Results: A anableps has 2 distinct optical systems in each eye: an upper one for aerial vision and a lower system for aquatic vision. These systems feature separate retinae and an asymmetric lens to achieve focus in the aerial and aquatic vision, but only 1 optic nerve per eye. The visual system is split horizontally to function optimally in a "prone" position in the water. D fuscus is a terrestrial feeder and has a vertically (almost perpendicular to the long axis of the fish) divided cornea using pigment and a condensation of collagen as the divider, a single pupil, and a divided retina. The split cornea allows for the fish to remain vertical with 1 cornea in air and 1 cornea in water. M macrocephalus is probably closely related to D fuscus with a similar split cornea. B exilis is a mesopelagic inhabitant living at approximately 200 to 1,000 m and has an ancillary globe that "buds" off the primary globe. This secondary globe is directed inferiorly toward the ocean floor as compared to the primary globe, which is directed 35° superiorly from the horizontal. Adult species of B exilis have 2 additional scleral bodies suspected to be lenses. If so, these structures would be capable of focusing light from the inferior field onto the superior retina, presumably adding to the panoramic inferior visual field. There are other mesopelagic species, including Styleophorus chordatus, Opisthoproctus grimaldii, Scopelarchus gantheri (or guentheri), Dolichopteryx binocularis, Benthalbella infans, and Evermannella indica, that have other unusual ocular mechanisms, such as retinal diverticulae and lens pads capable of reflection, but do not meet the definition of multiple eyes, as defined for purposes of this work. Conclusions: D fuscus and M macrocephalus are terrestrial feeders requiring aquatic and aerial vision, and hence have a split cornea for this purpose, and they probably use their anterior corneae for terrestrial vision. A anableps swims at the surface with combined aerial and aquatic vision for feeding and protection from predators. B exilis is a mesopelagic feeder requiring a binocular visual field in the horizontal meridian and above, and simultaneously is a bottom scavenger using an ancillary globe and perhaps scleral lenses for recognition of bioluminescent detritus. Although 2 of these models are related (D fuscus and M macrocephalus), these 4 fish represent 3 separate, distinct, and unrelated convergent evolutionary attempts toward 4 eyes in vertebrates satisfying the ecological needs of each. The 3 different models are unrelated evolutionarily and are found in 3 separate orders.

Original languageEnglish (US)
Pages (from-to)145-157
Number of pages13
JournalTransactions of the American Ophthalmological Society
Volume99
StatePublished - 2001

ASJC Scopus subject areas

  • Ophthalmology

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    Schwab, I. R., Ho, V., Roth, A., Blankenship, T. N., FitzGerald, P. G., & Yee, R. D. (2001). Evolutionary attempts at 4 eyes in vertebrates. Transactions of the American Ophthalmological Society, 99, 145-157.