Viruses Associated with Ovarian Degeneration in Apis mellifera L. Queens

Queen fecundity is a critical issue for the health of honeybee (Apis mellifera L.) colonies, as she is the only reproductive female in the colony and responsible for the constant renewal of the worker bee population. Any factor affecting the queen's fecundity will stagnate colony development, increasing its susceptibility to opportunistic pathogens. We discovered a pathology affecting the ovaries, characterized by a yellow discoloration concentrated in the apex of the ovaries resulting from degenerative lesions in the follicles. In extreme cases, marked by intense discoloration, the majority of the ovarioles were affected and these cases were universally associated with egg-laying deficiencies in the queens. Microscopic examination of the degenerated follicles showed extensive paracrystal lattices of 30 nm icosahedral viral particles. A cDNA library from degenerated ovaries contained a high frequency of deformed wing virus (DWV) and Varroa destructor virus 1 (VDV-1) sequences, two common and closely related honeybee Iflaviruses. These could also be identified by in situ hybridization in various parts of the ovary. A large-scale survey for 10 distinct honeybee viruses showed that DWV and VDV-1 were by far the most prevalent honeybee viruses in queen populations, with distinctly higher prevalence in mated queens (100% and 67%, respectively for DWV and VDV-1) than in virgin queens (37% and 0%, respectively). Since very high viral titres could be recorded in the ovaries and abdomens of both functional and deficient queens, no significant correlation could be made between viral titre and ovarian degeneration or egg-laying deficiency among the wider population of queens. Although our data suggest that DWV and VDV-1 have a role in extreme cases of ovarian degeneration, infection of the ovaries by these viruses does not necessarily result in ovarian degeneration, even at high titres, and additional factors are likely to be involved in this pathology.

蜂后繁殖力对于西方蜜蜂（Apis mellifera L.）蜂群的健康至关重要，因其是蜂群内唯一具备繁殖能力的雌性个体，且负责工蜂种群的持续更新。任何影响蜂后繁殖力的因素，都会阻滞蜂群的发育进程，并提升其对机会性致病菌（opportunistic pathogens）的易感性。我们发现了一种侵害卵巢的病变，其特征为卵巢顶端出现黄色变色，该现象由卵泡（follicles）的退行性损伤引发。在变色程度严重的极端病例中，多数卵巢小管（ovarioles）都会受到波及，此类病例均与蜂后的产卵缺陷存在关联。对退行性卵泡的显微观察显示，其中存在大量由30纳米二十面体病毒颗粒（icosahedral viral particles）构成的准晶体晶格（paracrystal lattices）。从退行性卵巢中构建的互补DNA（complementary DNA, cDNA）文库中，富集了大量变形翼病毒（deformed wing virus, DWV）与狄斯瓦螨病毒1（Varroa destructor virus 1, VDV-1）的序列——这两种均为常见且亲缘关系紧密的蜜蜂传染性软化病毒（Iflaviruses）。通过原位杂交（in situ hybridization）技术，也可在卵巢的多个部位检测到这两种病毒。针对10种不同蜜蜂病毒的大规模调查显示，DWV与VDV-1是蜂后种群中最为普遍的蜜蜂病毒；其在已交尾蜂后中的检出率（DWV为100%，VDV-1为67%）显著高于未交尾蜂后（DWV为37%，VDV-1为0%）。尽管在具有正常产卵功能与存在产卵缺陷的蜂后卵巢及腹部中，均可检测到极高的病毒载量（viral titres），但在更广范围的蜂后种群中，病毒载量与卵巢退行性病变或产卵缺陷之间并未存在显著相关性。尽管本研究数据显示，DWV与VDV-1在极端卵巢退行性病变病例中发挥了一定作用，但即便病毒载量极高，这两种病毒对卵巢的感染也未必会引发卵巢退行性病变，该病变的发生可能还涉及其他额外因素。