Data from: Sexual dimorphism and retinal mosaic diversification following the evolution of a violet receptor in butterflies

Numerous animal lineages have expanded and diversified the opsin-based photoreceptors in their eyes underlying color vision behavior. However, the selective pressures giving rise to new photoreceptors and their spectral tuning remain mostly obscure. Previously, we identified a violet receptor (UV2) that is the result of a UV opsin gene duplication specific to Heliconius butterflies. At the same time the violet receptor evolved, Heliconius evolved UV-yellow coloration on their wings, due to the pigment 3-hydroxykynurenine (3-OHK) and the nanostructure architecture of the scale cells. In order to better understand the selective pressures giving rise to the violet receptor, we characterized opsin expression patterns using immunostaining (14 species) and RNA-Seq (18 species), and reconstructed evolutionary histories of visual traits in five major lineages within Heliconius and one species from the genus Eueides. Opsin expression patterns are hyperdiverse within Heliconius. We identified six unique retinal mosaics and three distinct forms of sexual dimorphism based on ommatidial types within the genus Heliconius. Additionally, phylogenetic analysis revealed independent losses of opsin expression, pseudogenization events, and relaxation of selection on UVRh2 in one lineage. Despite this diversity, the newly evolved violet receptor is retained across most species and sexes surveyed. Discriminability modeling of behaviorally preferred 3-OHK yellow wing coloration suggests that the violet receptor may facilitate Heliconius color vision in the context of conspecific recognition. Our observations give insights into the selective pressures underlying the origins of new visual receptors.诸多动物演化支系均扩增并多样化了眼部内基于视蛋白（opsin）的光感受器，以此作为色觉行为的分子基础。然而，驱动新光感受器演化及其光谱调谐的选择压力，在很大程度上仍未明晰。此前我们已鉴定出一种紫光感受器（UV2），其源自仅存在于袖蝶属（Heliconius）蝴蝶中的紫外视蛋白基因复制事件。在该紫光感受器演化的同一时期，袖蝶属物种的翅膀也演化出了紫外黄色体色，这一特征由3-羟基犬尿氨酸（3-hydroxykynurenine, 3-OHK）色素以及鳞片细胞的纳米结构共同造就。为了更深入地解析驱动该紫光感受器演化的选择压力，我们通过免疫染色实验（覆盖14个物种）与RNA-Seq（覆盖18个物种）对袖蝶属的视蛋白表达模式进行了表征，并重建了袖蝶属内5个主要演化支以及1个邻纹蝶属（Eueides）物种的视觉性状演化历史。袖蝶属内的视蛋白表达模式呈现高度多样化。基于该属内的小眼类型，我们鉴定出6种独特的视网膜镶嵌模式以及3种不同的性二态形式。此外，系统发育分析显示，在其中一个演化支中存在视蛋白表达的独立丢失、假基因化事件，以及UVRh2基因所受选择压力的松弛。尽管存在上述多样化特征，新演化出的紫光感受器在本次研究所涉及的绝大多数袖蝶属物种以及不同性别中均得以保留。针对行为偏好的3-OHK黄色翅色进行的判别性建模分析表明，该紫光感受器可助力袖蝶属物种在同种识别场景下的色觉功能。本研究结果为解析新视觉感受器起源背后的选择压力提供了重要见解。