Simple and complex, sexually dimorphic retinal mosaic of fritillary butterflies

Butterflies have variable sets of spectral photoreceptors that underlie
colour vision. The photoreceptor organization may be optimised for the
detection of body colouration. Fritillaries (Argynnini) are nymphalid
butterflies exhibiting varying degrees of sexual dimorphism in wing
colouration. In two sister species, the females have orange (Argynnis
paphia) and dark wings (A. sagana), respectively, while the males of both
species have orange wings with large patches of pheromone-producing
androconia. In spite of the differences in female colouration, the eyes of
both species exhibit an identical sexual dimorphism. The female eyeshine
is uniform yellow, while the males have a complex retinal mosaic with
yellow and red-reflecting ommatidia. We found the basic set of UV-, blue-
and green-peaking photoreceptors in both sexes. Males additionally have
three more photoreceptor classes, peaking in the green, yellow and red,
respectively. The latter is the basal R9, indirectly measured through
hyperpolarisations in the green-peaking R1-2. In many nymphalid tribes,
including the closely related Heliconiini, the retinal mosaic is complex
in both sexes. We hypothesise that the simple mosaic of female Argynnini
is a secondary reduction, possibly driven by the use of olfaction for
intraspecific recognition, whereas vision remains the primary sense for
the task in the males.

蝴蝶拥有多样的光谱感光细胞组，这些细胞是其色觉的基础。感光细胞的组织方式可能经过优化，以适应对身体色彩的感知。豹蛱蝶（Argynnini族）属于蛱蝶科（Nymphalidae）蝴蝶，其翅色表现出不同程度的性二态性。在两个姐妹种中，雌性分别具有橙色翅膀（银豹蛱蝶Argynnis paphia）和深色翅膀（大豹蛱蝶A. sagana），而两个物种的雄性均拥有橙色翅膀，其上带有大片分泌信息素的性标（androconia）。尽管雌性翅色存在差异，但两个物种的复眼均表现出完全相同的性二态性。雌性复眼的反光呈均匀黄色，而雄性复眼则具有复杂的视网膜镶嵌结构，包含反射黄色和红色的小眼。我们在两种性别中均发现了基础的紫外、蓝色和绿色峰值感光细胞组。雄性还额外拥有三类感光细胞，其峰值分别位于绿色、黄色和红色光谱区域。其中后者（红色峰值感光细胞）为基底R9细胞，可通过绿色峰值R1-2细胞的超极化反应间接测量。在许多蛱蝶科族类中，包括亲缘关系较近的釉蛱蝶族（Heliconiini），雌雄两性的视网膜镶嵌结构均较为复杂。我们推测，豹蛱蝶族雌性的简单视网膜镶嵌结构是一种次生简化，其驱动因素可能是雌性依赖嗅觉进行种内识别，而雄性则仍以视觉作为该任务的主要感知方式。