Straying from the flatfish retinal plan: Cone photoreceptor patterning in the common sole (Solea solea) and the Senegalese sole (Solea senegalensis)

• Published in: Journal of comparative neurology (1911) 2020-10, Vol.528 (14), p.2283-2307
• Main Authors: Frau, Sara, Novales Flamarique, Iñigo, Keeley, Patrick W., Reese, Benjamin E., Muñoz‐Cueto, José A.
• Format: Article
• Language: English
• Subjects: Acuity; cone distributions; Cones; Mosaics; Nocturnal; opsin transcript; Periodicity; Photopigments; photoreceptor; Photoreceptors; Pleuronectiformes; Polymerase chain reaction; Retina; Species; Visual perception; visual pigment
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.24893

The retinas of nonmammalian vertebrates have cone photoreceptor mosaics that are often organized as highly patterned lattice‐like distributions. In fishes, the two main lattice‐like patterns are composed of double cones and single cones that are either assembled as interdigitized squares or as alternating rows. The functional significance of such orderly patterning is unknown. Here, the cone mosaics in two species of Soleidae flatfishes, the common sole and the Senegalese sole, were characterized and compared to those from other fishes to explore variability in cone patterning and how it may relate to visual function. The cone mosaics of the common sole and the Senegalese sole consisted of single, double, and triple cones in formations that differed from the traditional square mosaic pattern reported for other flatfishes in that no evidence of higher order periodicity was present. Furthermore, mean regularity indices for single and double cones were conspicuously lower than those of other fishes with “typical” square and row mosaics, but comparable to those of goldfish, a species with lattice‐like periodicity in its cone mosaic. Opsin transcripts detected by quantitative polymerase chain reaction (sws1, sws2, rh2.3, rh2.4, lws, and rh1) were uniformly expressed across the retina of the common sole but, in the Senegalese sole, sws2, rh2.4, and rh1 were more prevalent in the dorsal retina. Microspectrophotometry revealed five visual pigments in the retina of the common sole [S(472), M(523), M(536), L(559), and rod(511)] corresponding to the repertoire of transcripts quantified except for sws1. Overall, these results indicate a loss of cone mosaic patterning in species that are primarily nocturnal or dwell in low light environments as is the case for the common sole and the Senegalese sole. The corollary is that lattice‐like patterning of the cone mosaic may improve visual acuity. Ecological and physiological correlates derived from observations across multiple fish taxa that live in low light environments and do not possess lattice‐like cone mosaics are congruent with this claim. The retinas of many fishes are characterized by single and double cones that are organized into lattice‐like formations. The functional significance of such cone mosaic periodicity is unknown. Unlike other flatfishes, the common sole and the Senegalese sole lack lattice‐like organization of their cone mosaics. These findings suggest that square mosaics improve visual acuity and that