Pathogens may affect wing morphology in Apis mellifera (L.) workers

Geometric morphometrics is used to study the shape of biological structures through cartesian landmark coordinates. In honey bees, geometric morphometrics is typically applied to the bee forewings for subspecies identification. Both genetic and environmental factors may affect honey bee wing morphology, the latter including nutritional status, brood temperature, and Varroa infestation. Honey bees are threatened by several pathogens that can infect the juvenile stages, so impairing their development. Consequently, an effect on wing morphology can be postulated. This work aimed to investigate for the first time the effect of some major bee pathogens (DWV, KBV, ABPV, CBPV, and Nosema ceranae) on the honey bee wing morphology (size, shape, and fluctuating asymmetry). Honey bee worker forewings from six Italian regions were analysed. All the researched pathogens, as well as multiple infections, significantly affected both wing shape and size. DWV, the simultaneous co-infection with DWV, CBPV, and N. ceranae, and the total number of co-infecting pathogens were significantly associated with wing fluctuating asymmetry in both shape and size. In addition, N. ceranae was significantly associated with wing shape asymmetry. Our results showed that pathogens may affect honey bee wing morphology. However, we cannot rule out a colony-mediated effect on the impairment suffered by the individuals. Further experiments, including artificial infections, can help to clarify the importance of individual pathogens in the detected wing morphological alterations.

几何形态测量学（geometric morphometrics）通过笛卡尔地标坐标（cartesian landmark coordinates）研究生物结构的形态特征。在蜜蜂研究中，几何形态测量学通常被应用于蜜蜂前翅以开展亚种鉴定工作。遗传与环境因素均可影响蜜蜂翅形，其中环境因素涵盖营养状况、幼虫育幼温度以及瓦螨侵染。

蜜蜂面临多种可侵染其幼态阶段的病原体威胁，这些病原体会阻碍其发育，因此可推测这类病原体也会对翅形产生影响。本研究首次探究了数种主要蜜蜂病原体——变形翼病毒（DWV）、卡库戈病毒（KBV）、急性蜜蜂麻痹病毒（ABPV）、慢性蜜蜂麻痹病毒（CBPV）以及东方蜜蜂微孢子虫（Nosema ceranae）——对蜜蜂翅形（包括大小、形状与波动不对称性（fluctuating asymmetry））的影响。

本研究对采自意大利6个地区的工蜂前翅进行了分析。结果显示，所有被检测的病原体以及混合侵染均对翅形与翅大小产生了显著影响。其中，DWV单独侵染、DWV与CBPV及东方蜜蜂微孢子虫的共侵染，以及共侵染病原体的总数量，均与翅形和翅大小的波动不对称性显著相关。此外，东方蜜蜂微孢子虫也与翅形不对称性显著相关。

本研究结果表明，病原体可对蜜蜂翅形产生影响，但我们无法排除蜂群介导效应对个体所受损伤的作用。后续可开展包括人工侵染在内的相关实验，以明确各类单一病原体在所检测到的翅形改变中的具体作用。