Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies

Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies
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DOI:
10.1093/molbev/msx163
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发表时间:
2017-09-01
影响因子:
10.7
通讯作者:
Briscoe, Adriana D.
Briscoe, Adriana D.
中科院分区:
生物学1区
文献类型:
--
作者:
McCulloch, Kyle J.;Yuan, Furong;Briscoe, Adriana D.

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许多动物谱系都扩大了它们眼睛中基于视蛋白的光感受器并使其多样化,这些视蛋白是色觉行为的基础。然而,产生新光感受器的选择压力及其光谱调节仍然大多模糊。此前,我们发现了一种紫色受体 (UV2),它是 Heliconius 蝴蝶特有的 UV 视蛋白基因复制的结果。在紫色受体进化的同时,由于色素 3-羟基犬尿氨酸 (3-OHK) 和鳞片细胞的纳米结构,赫利康尼乌斯的翅膀也进化出了紫外黄色。为了更好地理解产生紫色受体的选择压力,我们使用免疫染色(14个物种)和RNA-Seq(18个物种)来表征视蛋白表达模式,并重建了Heliconius内的5个主要谱系和Eueides属的一个物种的视觉特征的进化历史。 Heliconius 内的视蛋白表达模式极其多样化。我们根据Heliconius属内的小眼类型确定了六种独特的视网膜镶嵌体和三种不同形式的性别二态性。此外,系统发育分析揭示了一个谱系中视蛋白表达的独立丢失、假发生事件以及 UVRh2 选择的放松。尽管存在这种多样性,但新进化的紫色受体在大多数接受调查的物种和性别中都保留了下来。行为偏好的 3-OHK 黄翅着色的可辨别性模型表明,紫色受体可能有助于同种识别背景下的 Heliconius 色觉。我们的观察深入了解了新视觉受体起源背后的选择压力。
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.