Genetic diversity can cause drastic effects on phenotypes and is commonly the result of a gene duplication event. Gene duplication and subsequent functional divergence of opsins, a G-protein coupled-receptor (GPCR), have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). Relatively few studies have been devoted to exploring the role of opsin duplication and evolution in non-arthropod invertebrates, and even fewer have integrated all the potential genetic diversity of opsins. In this dissertation, I utilized the photosensory system of the scallop, a marine bivalve, to study the evolution and expansion of the genetically diverse opsins, and demonstrate the complicated nature of Gq-opsin diversification after gene duplication. First, I explored how opsin paralogs diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians. Using a phylogenetic framework, I showed a pattern consistent with two rounds of duplication generating the four paralogous Gq-opsins in scallops. Differential expression of the four Gq-opsins across ocular and extra-ocular photosensitive tissues suggested that the Gq-opsins are used in different biological contexts in scallops, while protein modeling reveals variation in the amino acid composition, suggesting the four Gq-opsin paralogs may absorb different wavelengths of light. Second, I investigated how two Gq-opsin paralogs differentiate after a duplication event across the scallop family, Pectinidae. By comparing the rates of evolution between paralogous clades, I demonstrated both paralogs are under purifying selection, yet maintained at rates that are significantly different. I showed that one amino acid position, which is not considered a putative spectral tuning site, stands out as a strong candidate to explain the source of selection driving the difference in evolutionary rates. Finally, I discussed the current role of allelic variation in sensory systems and described how alleles are often discarded in studies of molecular evolution. I demonstrated the breadth of possible allelic variation within an individual and stressed the potential of cryptic genetic variation in the evolution of organisms by examining the allelic variation in Gq-opsins sampled across 34 bivalve species.