Context-Dependent Viral Transgenerational Immune Priming in Honey Bees (Hymenoptera: Apidae)

Abstract

Transgenerational immune priming is the process of increased resistance to infection in offspring due to parental pathogen exposure. Honey bees (Apis mellifera L. (Hymenoptera: Apidae)) are hosts to multiple pathogens, and this complex immune function could help protect against overwhelming infection. Honey bees have demonstrated transgenerational immune priming for the bacterial pathogen Paenibacillus larvae; however, evidence for viral transgenerational immune priming is lacking across insects in general. Here we test for the presence of transgenerational immune priming in honey bees with Deformed wing virus (DWV) by injecting pupae from DWV-exposed queens and measuring virus titer and immune gene expression. Our data suggest that there is evidence for viral transgenerational immune priming in honey bees, but it is highly context-dependent based on route of maternal exposure and potentially host genetics or epigenetic factors.

Lack of evidence for trans-generational immune priming against the honey bee pathogen Melissococcus plutonius

“…A difference in the expression of TGIP according to exposure route was also observed when honey bee queens were orally exposed to deformed wing virus or when injected with this virus [ 26 ]. This study suggested an interaction between the host genetics or epigenetics factors and the route of exposure in determining TGIP expression [ 26 ]. Such interactions could explain why other studies failed to orally induce TGIP in honey bee against the same inactivated virus [ 56 ].…”

“…TGIP expression thus may depend on the pathogen used for priming, host genetics, epigenetic factors or methodological issues such as the exposure procedure (e.g. [ 21 , 26 ]). Designing experiments to test the role of these factors and standardising experimental approaches are desirable to improve our understanding of TGIP mechanisms and their triggers.…”

“…Commonly occurring in vertebrates [ 22 ], TGIP was also shown to occur in invertebrates [ 23 ] and has been evidenced in all coleopteran, crustacean, orthopteran and mollusc species investigated to date [ 21 ]. Social Hymenoptera express TGIP against diverse pathogens, such as fungi (in the ants Formica fusca and Crematogaster scutellaris [ 24 , 25 ], viruses (in honey bees [ 26 ]) and bacteria (in bumble bees [ 27 – 30 ] and honey bees [ 31 , 32 ]). TGIP led to a significant increase in survival of their brood when honey bee queens were exposed to the pathogenic bacterium Paenibacillus larvae , which causes American foulbrood [ 31 ].…”

“…To consider potential TGIP-associated fitness costs to the queen and colony [ 33 ], which would jeopardise the economic sustainability of exploiting TGIP, we evaluated the impact of the procedure by measuring the survival and brood production of the queen in vivo . Because successful triggering of TGIP can depend on the experimental conditions of pathogen exposure [ 21 , 26 ], we also tested whether TGIP occurs naturally by comparing the survival to M . plutonius infection of brood produced by queens of EFB-diseased field colonies and of healthy colonies.…”

Viral Co-Infections and Antiviral Immunity in Honey Bees

“…The ‘suppressed in ovo viral infection’ (SOV) trait described by De Graaf et al [ 65 ] may result from transgenerational immune priming against DWV and may prevent its vertical transmission. However, the effects of queens’ DWV infection history on transgenerational immune priming still seems limited [ 66 ] and depended on multiple factors, including viral infection routes [ 67 ].…”