SignificanceOpsins are photosensitive receptors capturing specific wavelengths of incoming light to convey color vision across animals. Lack of reliable expression systems to study invertebrate G_qopsins has limited our ability to tease apart genotype–phenotype relationships underlying spectral tuning and visual adaptations in insects compared to homologous yet phylogenetically distant vertebrate G_topsin lineages. We developed a robust method to express invertebrate opsin proteins in vitro, which we apply to study the visual system of a lycaenid butterfly. Our detailed molecular characterization of red-shifted long-wavelength and duplicate short-wavelength G_qinsect opsins, together with a broad mutagenesis approach for exploring invertebrate opsin sequence-visual pigment functions, begins pinpointing the proximate evolutionary mechanisms underlying the diversification of color vision systems across animal life.