Single cones give rise to multi-cone types in the retinas of fishes

Retinal cone photoreceptors are specialized neurons that capture light to begin the process of daylight vision. They occur as individual cells (i.e., single cones), or as combinations of structurally linked cells, such as the double and triple cones found in the retinas of non-eutherian vertebrates. These different morphological cone types form mosaics of varying regularity, with single and double cones patterned as nearly perfect lattices in the retinas of many bony fishes (teleosts) and some geckos. Although double cones were first reported over 150 years ago, how they form (i.e., whether from coalescing single cones, or from structurally linked cone progenitors) remains uncertain. In turn, whether there is a general vertebrate sequence in appearance of morphological cone types and mosaics is unknown. Here, the developing retinas of seven species of teleosts were examined revealing that only single cones, arranged in hexagonal-like mosaics, were present at the earliest stages of photoreceptor differentiation. Double cones arose from coalescing single cones and the formation of multi-cone type mosaics (such as the square mosaic, where each single cone is surrounded by four double cones) followed different dynamics depending on whether the species was altricial or precocial. Single cones were therefore the primordial cells from which all multi-cone types arose and hexagonal-like mosaics preceded other mosaic patterns. Based on observations from transitional retinas, we propose a model for mosaic transformation from hexagonal to square. The double cones of fishes and those of land vertebrates constitute an example of convergent evolution to achieve the elliptical waveguide structure, likely for improved spatio-temporal resolution.