It is a widespread practice in China to keep colonies of both the western honey bee, Apis mellifera, and the eastern honey bee, Apis cerana, in close proximity. However, this practice increases opportunities for spillover of parasites and pathogens between the two host bee species, impacting spatial and temporal patterns in the occurrence and prevalence of the viruses that adversely affect bee health. We conducted a 1‐year large‐scale survey to assess the current status of viral infection in both A. mellifera and A. cerana in China. Our study focused on multiple aspects of viral infections in honey bees, including infection rate, viral load, seasonal variation, regional variation, and phylogenetic relationships of the viruses within the same species found in this study and other parts of the world. The survey showed that the black queen cell virus (BQCV), deformed wing virus (DWV), Israeli acute paralysis virus (IAPV), and sacbrood virus (SBV) were common in both A. mellifera and A. cerana, and infection dynamics of BQCV, DWV, and SBV between bee species or seasons were significantly different. DWV was the most common virus in A. mellifera, and its infection rate and load in A. mellifera were higher than those in A. cerana, which reflects the high susceptibility of A. mellifera to Varroa destructor infestation. The infection rate and viral load of SBV were higher in A. cerana than in A. mellifera, indicating that SBV poses a greater threat to A. cerana than to A. mellifera. Our results also suggested that there was no geographical variation in viral dynamics in A. mellifera and A. cerana. Phylogenetic analyses of BQCV, DWV, IAPV, and SBV suggested the cross‐regional and cross‐species spread of these viruses. This study provides important insights into the complex relationships between viruses and their hosts in different seasons and regions, which will be important for developing effective disease management strategies to improve bee health.

The ability to synthesize essential molecules is sometimes lost in evolution. A classic example is ascorbate (vitamin C), which is synthesized in most animals by L-gulonolactone oxidase (GULO), an enzyme lost multiple independent times in animal evolution. This event is thought to be evolutionarily neutral; however, GULO- deficient animals including humans need to obtain ascorbate from their diet and are prone to ascorbate deficiency and scurvy. We therefore hypothesized that this disadvantage of GULO loss is offset by physiological benefits. Here, we show that ascorbate deficiency benefits mice infected with schistosome parasites, which cause schistosomiasis, a debilitating parasitic disease that afflicts 250 million people. Schistosoma mansoni worms required host ascorbate to produce eggs in vivo. Consequently, ascorbate-deficient mice were protected from schistosomiasis pathologies and transmission. Intermittent ascorbate deficiency protected Gulo -deficient mice from both scurvy and schistosomiasis mortality. The effects of ascorbate on schistosome reproduction were mediated by ascorbate-dependent histone demethylation which promoted vitellocyte development in female schistosomes. We propose that vitamin deficiencies are not always detrimental but can protect animals from pathogens which need to obtain vitamins from their host.

Egg production by female schistosomes drives both transmission and pathology of schistosomiasis, affecting over 200 million people. Female maturation relies on the male-derived pheromone β-alanyl-tryptamine (BATT), but underlying molecular mechanisms are unclear. We identified the BATT-responsive transcription factor gene znf362 as a key regulator of female reproductive development. Functional studies showed that znf362.1 , but not znf362.2 , is essential for BATT-induced ovary and vitellaria maturation. Single-cell transcriptomics and in situ hybridization revealed up-regulation of znf362.1 in oocytes and vitellaria S ₁ cells after BATT exposure. Multiomics analysis showed ZNF362.1 directly activates Smp_349410 , a female gonad-specific gene encoding a CPEB1 homolog. Loss of znf362.1 or Smp_349410 impaired oocyte and vitellocyte differentiation without affecting progenitors. Mechanistically, Sm CPEB1 promotes female ovary development by regulating polyadenylation of cyclin B1 mRNA and drives S ₁ cell differentiation in the vitellaria. These findings define a transcriptional and post-transcriptional axis, BATT- znf362.1 - cpeb1 , that initiates female sexual maturation, offering mechanistic insight into schistosome reproduction and potential targets for schistosomiasis control.