Data from: UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication

Mimetic wing coloration evolves in butterflies in the context of predator confusion. Unless butterfly eyes have adaptations for discriminating mimetic color variation, mimicry also carries a risk of confusion for the butterflies themselves. Heliconius butterfly eyes, which express recently duplicated UV opsins, have such an adaptation. To examine bird and butterfly color vision as sources of selection on butterfly coloration we studied yellow wing pigmentation in the tribe Heliconiini. We confirmed using reflectance and mass spectrometry that only Heliconius use 3-hydroxy-DL kynurenine (3-OHK) as a wing pigment. 3-OHK looks yellow to humans but it reflects both UV- and long-wavelength light whereas butterflies in related genera have chemically unknown yellow pigments mostly lacking UV-reflectance. Modeling of these color signals reveals that the two UV photoreceptors of Heliconius are better suited to separating 3-OHK from non-3-OHK spectra compared to the photoreceptors of related genera or birds. The co-occurrence of potentially enhanced UV-vision and a UV-reflecting ‘yellow’ wing pigment could allow unpalatable Heliconius private intraspecific communication in the presence of mimics. Our results are the best available evidence for the correlated evolution of a color signal and color vision. They also suggest that predator visual systems are error-prone in the context of mimicry.

蝴蝶的拟态翅色演化以混淆捕食者识别为选择背景。若蝴蝶眼部未演化出区分拟态色彩差异的适应机制，拟态本身也会给蝴蝶自身带来识别混淆的风险。表达近期复制型紫外视蛋白（UV opsins）的釉蛱蝶（Heliconius）眼部便具备这类适应机制。为探究鸟类与蝴蝶的色觉作为蝴蝶翅色演化选择压力的作用，我们对釉蛱蝶族（Heliconiini）的黄色翅色素展开了研究。我们通过反射光度法与质谱分析法证实，仅釉蛱蝶属物种以3-羟基-DL-犬尿氨酸（3-hydroxy-DL kynurenine，3-OHK）作为翅色素。3-OHK在人类视觉中呈现黄色，但其可反射紫外与长波光线；而近缘属蝴蝶的黄色翅色素化学成分尚不明确，且大多不具备紫外反射特性。对上述色彩信号的建模分析显示，与近缘属蝴蝶或鸟类的光感受器相比，釉蛱蝶的两类紫外光感受器更擅长区分3-OHK与非3-OHK的光谱特征。潜在增强的紫外视觉与具备紫外反射特性的‘黄色’翅色素二者的协同存在，可使具有不可食用性的釉蛱蝶在拟态者存在的情况下，实现专属的种内通讯。本研究结果是目前关于色彩信号与色觉协同演化的最有力实证，同时也表明捕食者的视觉系统在拟态场景中存在识别误差。