Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake

Dec 31, 2015Proceedings of the National Academy of Sciences of the United States of America

Changes in rod light-detecting cells in the all-cone eye of a daytime-active garter snake

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Abstract

Evidence suggests that garter snake photoreceptors may be modified rods rather than true cones.

The study investigates the evolutionary fate of rod photoreceptors in a diurnal garter snake.
Findings indicate the presence of a functional, blue-shifted rhodopsin in small single 'cones.'
These 'cones' express rod transducin and exhibit ultrastructural features typical of rods.
The data supports the idea that these modified rods evolved to enhance spectral sensitivity and color discrimination.
The results may illustrate how sensory evolution is influenced by both environmental factors and historical changes.

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Vertebrate retinas are generally composed of rod (dim-light) and cone (bright-light) photoreceptors with distinct morphologies that evolved as adaptations to nocturnal/crepuscular and diurnal light environments. Over 70 years ago, the "transmutation" theory was proposed to explain some of the rare exceptions in which a photoreceptor type is missing, suggesting that photoreceptors could evolutionarily transition between cell types. Although studies have shown support for this theory in nocturnal geckos, the origins of all-cone retinas, such as those found in diurnal colubrid snakes, remain a mystery. Here we investigate the evolutionary fate of the rods in a diurnal garter snake and test two competing hypotheses: (i) that the rods, and their corresponding molecular machinery, were lost or (ii) that the rods were evolutionarily modified to resemble, and function, as cones. Using multiple approaches, we find evidence for a functional and unusually blue-shifted rhodopsin that is expressed in small single "cones." Moreover, these cones express rod transducin and have rod ultrastructural features, providing strong support for the hypothesis that they are not true cones, as previously thought, but rather are modified rods. Several intriguing features of garter snake rhodopsin are suggestive of a more cone-like function. We propose that these cone-like rods may have evolved to regain spectral sensitivity and chromatic discrimination as a result of ancestral losses of middle-wavelength cone opsins in early snake evolution. This study illustrates how sensory evolution can be shaped not only by environmental constraints but also by historical contingency in forming new cell types with convergent functionality.

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Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake

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