Morphology, Characterization and Distribution of Retinal Photoreceptors in the South American (Lepidosiren paradoxa) and Spotted African (Protopterus dolloi) Lungfishes

Abstract

Lungfishes are the closest living relatives of the ancestors to all terrestrial vertebrates and have remained relatively unchanged since the early Lochkovin period (410 mya). Lungfishes, therefore, represent a critical stage in vertebrate evolution and their sensory neurobiology is of considerable interest. This study examines the ultrastructure of the retina of two species of lungfishes: the South American lungfish, Lepidosiren paradoxa and the spotted African lungfish, Protopterus dolloi in an attempt to assess variations in photoreception in these two ancient groups of sarcopterygian (lobe-finned) fishes. In juvenile P. dolloi, the retina contains one rod and two cone photoreceptor types (one containing a red oil droplet), while only one rod and one cone photoreceptor type is present in adult L. paradoxa. Both species lack double cones. The large size and inclusion of oil droplets in both species apart from one of the cone photoreceptor types in P. dolloi suggests that L. paradoxa and P. dolloi are adapted for increasing sensitivity. However, the complement of photoreceptor types suggests that there may be a major difference in the capacity to discriminate color (dichromatic and monochromatic photoreception in P. dolloi and L. paradoxa, respectively). This study suggests that the visual needs of these two species may differ.

Evolution, Development and Function of Vertebrate Cone Oil Droplets

“…The complete loss of oil droplets in certain dim-light clades (e.g., snakes, eutherian mammals) suggests that the light-collecting function may be of marginal utility in low-light environments (Walls, 1942 ). In further support of this notion, oil droplets have only rarely been observed in rods (Walls, 1942 ; Appudurai et al, 2016 ). Spatial summation and convergence of multiple rod signals onto a single retinal ganglion cell may suffice to enhance sensitivity in dim environments, thus rendering oil droplets superfluous.…”

“…The chemical composition of these oil droplets has not been investigated, but the spectral properties of the red droplets are similar to the astaxanthin-pigmented droplets of turtles and birds. The spotted African lungfish ( Protopterus dolloi ) has a single cone photoreceptor containing a red oil droplet, another cone subtype without an oil droplet, and a colorless oil droplet within their rod photoreceptors (Appudurai et al, 2016 ). The rod and cone photoreceptors of the South American lungfish ( Lepidosiren paradoxa ) both contain colorless oil droplets, and it is speculated that this species may be less dependent on color vision than other lungfishes (Ali and Anctil, 1973 ; Appudurai et al, 2016 ).…”

“…The spotted African lungfish ( Protopterus dolloi ) has a single cone photoreceptor containing a red oil droplet, another cone subtype without an oil droplet, and a colorless oil droplet within their rod photoreceptors (Appudurai et al, 2016 ). The rod and cone photoreceptors of the South American lungfish ( Lepidosiren paradoxa ) both contain colorless oil droplets, and it is speculated that this species may be less dependent on color vision than other lungfishes (Ali and Anctil, 1973 ; Appudurai et al, 2016 ). The presence of oil droplets in the rod photoreceptors is surprising, given their absence from the rods of the majority of other taxa.…”

<strong>&shy;</strong>The Retinal Basis of Vertebrate Color Vision

“…For example, some fish corneas transmit UV while others absorb short wavelengths (Siebeck & Marshall 2001). Spectral filtering is however most significant in those groups whose cone inner segments contain colored oil droplets, namely a lungfish, birds and certain reptiles, including freshwater turtles and lizards (Appudurai et al 2016, Hart 2001, Loew et al 2002 (Fig. 2c).…”

Morphology of the cornea and iris in the Australian lungfish Neoceratodus forsteri (Krefft 1870) (Dipnoi): Functional and evolutionary perspectives of transitioning from an aquatic to a terrestrial environment

“…According to Appudurai et al (2016), colour discrimination in South American (L. paradoxa) and spotted African (P. dolloi) lungfishes may be different from N. forsteri, where there are species-specific differences in the complement of retinal photoreceptors (one rod and two cone types in P. dolloi and one rod and one type of cone in L.…”