The Interactions between Hygienic Behavior, Immune Response, and Virus Infection in Honeybees

Honey bee colonies are prone to invasion by pests and pathogens. The combination of the parasitic mite Varroa destructor ( Varroa ) and the multiple viruses it vectors, is a major driver of colony losses. Breeding for hygienic behavior to reduce Varroa populations is considered a sustainable way to reduce the impact of Varroa on honey bee health. However, hygienic behavior may have a cost to the health of individual bees, both in terms of viral infection risk and immune function. To determine whether selection for hygienic behavior at the colony level is associated with trade-offs in honey bee viral infection and immune function, we compared Varroa infestation, viral loads, and individual immune function between honey bee colonies that were bred for high and low hygienic behavior. Specifically, we measured Varroa infestation, DWV A, DWV B, ABPV, and IAPV viral genome levels in bee samples from colonies with artificially inseminated queens in our bi-directional selection program for hygienic behavior in Israel. In addition, we evaluated the expression of 12 genes from the Jak-STAT, Toll, Imd and RNAi immune pathways. We found significantly lower Varroa infestation and DWV loads in highly hygienic colonies than in colonies exhibiting low hygienic behavior. In addition, workers of the hygienic colonies had significantly higher expression of the immune genes PGRP-S2 and hymenoptaecin compared to workers from low hygienic colonies. These results indicate no trade-offs in breeding for hygienic behavior: Hygienic honey bees were associated with reduced Varroa populations and reduced viral prevalence and load at the colony level. Individual immunity of hygienic bees was increased, which could explain lower virus levels, although lower Varroa levels due to social immunity are likely to contribute as well. In sum, we demonstrate multiple health benefits of breeding for honey bee hygiene.