Invertebrate predators attack eyespots and promote the evolution of phenotypic plasticity

Some eyespots are thought to deflect attack away from the vulnerable body, yet there is limited empirical evidence for this function and its adaptive advantage. Here, we demonstrate the conspicuous ventral hindwing eyespots found on Bicyclus anynana butterflies protect against invertebrate predators, specifically praying mantids. Wet season (WS) butterflies with larger, brighter eyespots were easier for mantids to detect, but more difficult to capture compared to dry season (DS) butterflies with small, dull eyespots. Mantids attacked the wing eyespots of WS butterflies more frequently resulting in greater butterfly survival and reproductive success. With a reciprocal eyespot transplant, we demonstrated the fitness benefits of eyespots were independent of butterfly behaviour. Regardless of whether the butterfly was WS or DS, large marginal eyespots pasted on the hindwings increased butterfly survival and successful oviposition during predation encounters. In previous studies, DS B. anynana experienced delayed detection by vertebrate predators, but both forms suffered low survival once detected. Our results suggest predator abundance, identity and phenology may all be important selective forces for B. anynana. Thus, reciprocal selection between invertebrate and vertebrate predators across seasons may contribute to the evolution of the B. anynana polyphenism.

人们普遍认为眼斑（eyespots）可将攻击引离蝴蝶脆弱的躯体，但目前针对该功能及其适应性优势的实证证据仍较为匮乏。本研究证实，凡那矍眼蝶（Bicyclus anynana）后翅腹面显著的眼斑可抵御无脊椎动物捕食者，尤其是螳螂。湿季型（WS）个体的眼斑更大更鲜亮，虽更易被螳螂察觉，但相较于眼斑小巧黯淡的干季型（DS）个体，更难被捕获。螳螂更频繁地攻击湿季型个体的翅部眼斑，从而使该类蝴蝶的存活率与繁殖成功率更高。通过反向眼斑移植实验，我们证实眼斑带来的适合度（fitness）优势与蝴蝶自身行为无关。无论个体属于湿季型还是干季型，粘贴于后翅的大型边缘眼斑均可提升捕食遭遇场景下的蝴蝶存活率与成功产卵率。过往研究显示，干季型的凡那矍眼蝶被脊椎动物捕食者察觉的时间更晚，但两类个体一旦被发现，存活率均较低。本研究结果表明，捕食者的丰度、类群与物候期，均可能是影响凡那矍眼蝶的重要选择压力。因此，跨季节的无脊椎与脊椎动物捕食者之间的反向选择，可能推动了凡那矍眼蝶表型多型（polyphenism）的演化。