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，其核心选择背景为干扰捕食者的视觉辨识。倘若蝴蝶眼部未演化出区分拟态色彩差异的适应性机制，则拟态本身也可能给蝴蝶自身带来视觉混淆的风险。表达新近复制的紫外视蛋白（UV opsins）的釉蛱蝶属（Heliconius）眼部，便具备这类适应性视觉特征。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）的黄色翅部色素展开了研究。我们通过反射光谱法与质谱法证实，仅釉蛱蝶属（Heliconius）会以3-羟基-DL-犬尿氨酸（3-hydroxy-DL kynurenine，简称3-OHK）作为翅部色素。3-OHK在人类视觉中呈现黄色，但可同时反射紫外与长波长光线；而近缘属蝴蝶的黄色翅色素化学成分尚未明确，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，相较于近缘属蝴蝶或鸟类的光感受器，釉蛱蝶属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。潜在增强型紫外视觉与紫外反射型‘黄色’翅色素的协同存在，可让有毒的釉蛱蝶在拟态者共存的环境中，依然能够进行种内私密通讯。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证据，同时也表明，在拟态情境下，捕食者的视觉系统存在视觉辨识误差的可能性。