A lens with a graded refractive index is required for vision in aquatic animals with camera-type eyes. This optical design entails a radial gradient of protein density, with low density in external layers, and high density in internal layers. To maintain the optical stability of the eye, different material properties are required of proteins in different regions of the lens. In low-density regions of the lens where slight protein aggregation causes significant light scattering, aggregation must be minimized. Animal lenses are made primarily of high concentrations of proteins called lens crystallins. Squid lens S-crystallin proteins are evolutionarily derived from the glutathione s-transferase protein family. We used biochemistry, optical modeling, and phylogenetics to study the evolution and material properties of S-crystallins. S-crystallins are differentially expressed in a radial gradient, suggesting a role in refractive index. This gradient in S-crystallin expression is correlated with their evolutionary history and biochemistry. S-crystallins have been under positive selection. This selection appears to have resulted in stabilization of derived S-crystallins via mutations in the dimer interface and extended electrostatic fields. These derived S-crystallins likely cause the glassy organization and stability of low refractive index lens layers. To understand the physiological implications of this protein evolution in squid ecology, the modulation transfer function of eight species of mesopelagic cephalopod was measured. The optical capabilities of cephalopods lenses vary, with the pelagic octopus Japatella diaphana having a less acute lens than decapod squid. The vampyromorph squid Vampyroteuthis infernalis possesses an extremely acute lens, approaching or equal to the optical system of humans.