Abstract

Sequence-specific gene silencing mechanisms, including RNA interference (RNAi), are induced and maintained by the presence of double stranded RNA (dsRNA). Systemic RNAi initiated by artificial dsRNA ingestion has been reported in diverse invertebrates, including honeybees, demonstrating environmental RNAi up-take and impact on the whole organism level. However, the question why any organism would take up RNA from the environment has remained unanswered. Here, we report on horizontal transfer of silencing RNAs among individual honeybees mediated by ingestion of worker and royal jelly diets. We show that ingested dsRNA can be detected in the honeybee’s hemolymph associated with a protein complex. Furthermore, RNA extracted from worker and royal jelly exposed a differential natural occurrence of RNA populations. Some of these RNAs corresponded to honeybee protein coding genes, transposable elements, non-coding RNA and exogenous viruses. Finally, we identified and characterized a nucleic acid binding royal jelly protein that binds RNA longer than 20 nt in a non-sequence specific manner. Remarkably, RNA binding mediates higher order assembly of the protein, leading to the formation of large ribonucleoprotein complexes that protect RNA from degradation and enhance ingested RNA uptake. A transmissible RNA pathway and its potential roles in social immunity and epigenetic dynamics among honeybees and potentially other close interacting individuals will be discussed.