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Why are the retinal color receptors cone-shaped? This is not a trivial question: the cone shape is evidently a universal feature of the color receptors while the achromatic rod receptors are always rod-shaped. What might be behind this dichotomy has not previously been explored in any meaningful way. We suggest here that the cone shape is not an incidental feature, but actually integral to cone function. We describe a waveguide mode cut-off effect that can physically separate light into its spectral colors along the length of a small, tapered waveguide, i.e., a cone. This effect converts the spectrum of incident light into position-dependent information along a tapered fiber; long-wavelength red light is excluded from the cone first, and the shortest-wavelength, blue light last. The retinal cone optical dimensions are apparently ideally tuned to exhibit this spectral dispersion. Converting this length-correlated information into a readable color code can be accomplished through translation into a time-correlated code through the microsaccadic movements of the eye to synchronize the time-delayed electrical signal generated by photoabsorption events from different positions along the receptor. Such a time code explains the existence of subjective color effects such as that induced by Benham’s Top. Detecting color information through such a waveguide effect also explains the Stiles-Crawford Effect of the Second Kind (SC II) whereby the apparent color of monochromatic light depends on its angle of incidence at the retina. The long puzzling similarity of violet and purple is directly explained by excitation of second-order waveguide mode propagation for short-wavelength light in this model. This dynamic model of color vision also accounts for the breakdown of statically-established metameric color matches under dynamic presentation, a feature of color vision that contradicts the basic assumptions of the standard Young-Helmholtz trichromatic model. Further underscoring the utility of the our proposed model is that it explains the major features of common forms of color blindness as a consequence of “mistuning” of the cone parameters.