Patterns in Teleost Photoreceptor Organization: A Characterization of Basal Body Positioning in Zebrafish Photoreceptors and Variations in Swordtail Photoreceptor Mosaics



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Vertebrate vision is enabled by light-sensitive photoreceptors arranged in a plane in the retina. This study investigates two aspects of this arrangement: 1) positioning of basal bodies within photoreceptors, and 2) positioning of photoreceptors themselves. First, the planar cell polarity of basal bodies, and therefore cilia, is often critical for proper cilia function and is controlled by the planar cell polarity (PCP) pathway. Cilia planar positioning in vertebrate photoreceptors, however, has not been characterized. Because zebrafish photoreceptors form an organized, well-characterized mosaic, they are an ideal system to address photoreceptor basal body positioning. Second, swordtail fish are frequently studied to investigate visually-mediated social behaviors such as mate choice and how these influence evolution. However, less is known about the morphology of their photoreceptor mosaic and how this mosaic influences behavior. Therefore, characterization of the swordtail photoreceptor mosaic is an important step in understanding this relationship between physiology and behavior. In this study, immunohistology is used to characterize cryosectioned flatmounted retinas from zebrafish and swordtails with various genetic, behavioral, and environmental backgrounds.

The results of this study reveal that in adult zebrafish retinas, the basal bodies of red-, green-, and blue-sensitive cone photoreceptors localize asymmetrically on the cell edge nearest the optic nerve. In contrast, no patterning is in the basal bodies of ultraviolet-sensitive cones, of rod photoreceptors, or of larval cones. Both rod loss and UV-light addition do not affect cone basal body patterning. Darkness during development leads to bimodality of basal bodies. These results suggest that, after the transition to the adult mosaic, a cellular mechanism involving cell-cell contact, consistent with the PCP pathway, regulates photoreceptor basal body positioning.

The results of this study also reveal that the swordtails Xiphophorus malinche, Xiphophorus birchmanni, and their hybrids exhibit an organized square mosaic, although some variations in this pattern exist, including between males and females. As square mosaics have been correlated with sensitivity to changes in light polarization, this warrants future studies in swordtail polarization vision, which may play an important role in visually-mediated behavior. Also, changes in the photoreceptor mosaic might have explanatory power for changes in visually-mediated behavior.