Suspension and optical properties of the crystalline lens in the eyes of basal vertebrates.

We have investigated the apparatus suspending the crystalline lens in the eyes of basal vertebrates. Data are presented for Holocephali (Chondrichthyes) and the actinopterygians Polypteriformes, Polyodontidae (Acipenseriformes), Lepisosteiformes, Amiiformes, and one teleost species, the banded archerfish (Toxotes jaculatrix). We also studied the optical properties of the lens in Polypteriformes, Lepisosteiformes, and the archerfish. Together with previously published results, our findings show that there are three basic types of lens suspension in vertebrates. These are i) a rotationally symmetric suspension (Petromyzontida, lampreys; Ceratodontiformes, lungfishes; Tetrapoda), ii) a suspension with a dorso-ventral axis of symmetry and a ventral papilla (all Chondrichthyes and Acipenseriformes), and iii) an asymmetric suspension with a ventral muscle and a varying number of ligaments (all Actinopterygii except for Acipenseriformes). Large eyes with presumably high spatial resolution have evolved in all groups. Multifocal lenses creating well-focused color images are also present in all groups studied. Stable and exact positioning of the lens, in many cases in combination with accommodative changes in lens position or shape, is achieved by all three types of lens suspension. It is somewhat surprising that lens suspensions are strikingly similar in Chondrichthyes and Acipenseriformes (Actinopterygii), while the suspension apparatus in Polypteriformes, usually being regarded as an actinopterygian group more basal than Acipenseriformes, are considerably more teleostean-like. This study completes a series of investigations on lens suspensions in nontetrapod vertebrates, covering all major groups except for the rare and highly derived coelacanths.

Sturgeons, sharks, and rays have multifocal crystalline lenses and similar lens suspension apparatuses.

Crystalline lenses with multiple focal lengths in monochromatic light (multifocal lenses) are present in many vertebrate groups. These lenses compensate for chromatic aberration and create well-focused color images. Stabilization of the lens within the eye and the ability to adjust focus are further requirements for vision in high detail. We investigated the occurrence of multifocal lenses by photorefractometry and lens suspension structures by light and electron microscopy in sturgeons (Acipenseriformes, Chondrostei) as well as sharks and rays (Elasmobranchii, Chondrichthyes). Multifocal lenses were found in two more major vertebrate groups, the Chondrostei represented by Acipenseriformes and Chondrichthyes represented by Elasmobranchii. The lens suspension structures of sturgeons, sharks, and rays are more complex than described previously. The lens is suspended by many delicate suspensory fibers in association with a ventral papilla in all groups studied. The arrangements of the suspensory fibers are most similar between sturgeons and sharks. In rays, the lens is suspended by a smaller ventral papilla and the suspensory fibers are arranged more concentrically to the lens.

A fibrous membrane suspends the multifocal lens in the eyes of lampreys and African lungfishes.

The sharpness and thus information content of the retinal image in the eye depends on the optical quality of the lens and its accurate positioning in the eye. Multifocal lenses create well-focused color images and are present in the eyes of all vertebrate groups studied to date (mammals, reptiles including birds, amphibians, and ray-finned fishes) and occur even in lampreys, i.e., the most basal vertebrates with well-developed eyes. Results from photoretinoscopy obtained in this study indicate that the Dipnoi (lungfishes), i.e., the closest piscine relatives to tetrapods, also possess multifocal lenses. Suspension of the lens is complex and sophisticated in teleosts (bony fishes) and tetrapods. We studied lens suspension using light and electron microscopy in one species of lamprey (Lampetra fluviatilis) and two species of African lungfish (Protopterus aethiopicus aethiopicus and Protopterus annectens annectens). A fibrous and highly transparent membrane suspends the lens in both of these phylogenetically widely separated vertebrate groups. The membrane attaches to the lens approximately along the lens equator, from where it extends to the ora retinalis. The material forming the membrane is similar in ultrastructure to microfibrils in the zonule fibers of tetrapods. The membrane, possibly in conjunction with the cornea, iris, and vitreous body, seems suitable for keeping the lens in the correct position for well-focused imaging. Suspension of the lens by a multitude of zonule fibers in tetrapods may have evolved from a suspensory membrane similar to that in extant African lungfishes, a structure that seems to have appeared first in the lamprey-like ancestors of allextant vertebrates.