THE SNAKE RETINA – A FASCINATING MODEL OF ADAPTIONS AND PARALLEL EVOLUTION IN NOCTURNAL VERTEBRATES
1 Max-Planck Institute for Neurobiology of Behavior, Bonn, Germany
2 University of São Paulo, São Paulo, BR
3 Charles University, Prague, Czech Republic
4 Natural History Museum, London, UK
The more than 4,000 living species of snakes comprise a fascinating, ecomorphologically diverse group of vertebrates with astonishing retinas. Snakes have greatly variable visual cells and retinal patterns, and multiple evolutionary transitions between diurnal and nocturnal activity makes them an ideal group to test hypotheses on visual adaptations to diverse diel activity patterns. In ‘basal’ snakes (henophidians), dim-light activity correlates with a high density of rods containing the rhodopsin photopigment (RH1), along with LWS- and SWS1-single cones. In ‘advanced’ snakes (caenophidians), differences in diel activity are accompanied by extreme adaptations of the outer retina. Nocturnal species have duplex retinas, similar to those of henophidians but with an additional, double LWS cone. Diurnal species have peculiar “all-cone” retinas, with four cone types, one of which is a modified rod. Employing a comparative approach within a phylogenetic framework, we used immunohistochemistry and electron microscopy to investigate photoreceptor terminals and their connectivity with bipolar cells. We identified several immunohistochemical markers for snake bipolar cells, some of which are lineage-specific, and some that display differential labeling patterns in duplex and all-cone retinas. In particular, PKC-a labeling revealed a rod-selective ON bipolar cell in nocturnal snakes, and an LWS-cone-selective bipolar cell in “all-cone” retinas of diurnal species. Our findings reveal divergences in the retinal architecture of diurnal and nocturnal snakes and provide a first view into the initial steps of visual processing in this diverse and understudied group. Large-scale EM reconstruction allows us to investigate the rod pathway in a nocturnal snake and search for a comparable pathway in a diurnal snake.