Exposure to Inactivated Deformed Wing Virus Leads to Trans-Generational Costs but Not Immune Priming in Honeybees (Apis mellifera)

Abstract

Pathogens are identified as one of the major drivers behind the honeybee colony losses, as well as one of the reasons for the reported declines in terrestrial insect abundances in recent decades. To fight infections, animals rely on their immune system. The immune system of many invertebrates can be primed by exposure to a pathogen, so that upon further exposure the animal is better protected. The protective priming effect can even extend to the next generation, but the species capable of priming the immune system of their offspring are still being investigated. Here we studied whether honeybees could prime their offspring against a viral pathogen, by challenging honeybee queens orally with an inactivated deformed wing virus (DWV), one of the most devastating honeybee viruses. The offspring were then infected by viral injection. The effects of immune priming were assayed by measuring viral loads and two typical symptoms of the virus, pupal mortality, and abnormal wing phenotype. We saw a low amount of wing deformities and low pupal mortality. While no clear priming effect against the virus was seen, we found that the maternal immune challenge, when combined with the stress caused by an injection during development, manifested in costs in the offspring, leading to an increased number of deformed wings.

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

“…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 ]. Such contrasting results are not specific to honey bees and have been reported for Diptera and Lepidoptera.…”

Dynamics in vertical transmission of viruses in naturally selected and traditionally managed honey bee colonies across Europe

“…Immune priming refers to responses specific to the pathogen whereas immune enhancement refers to responses non-specific to the pathogen [117]. Trans-generational immune priming has been described in honey bees for American foulbrood [118,119] along with its associated cost [120]. The reduced vertical transmission with age and between seasons for DWV and not for BQCV suggests that immune priming also occurs in honey bee queens within generations, as has been found in other insects [reviewed by 104,106,108].…”

Reproductive consequences of transient pathogen exposure across host genotypes and generations

“…Across host species, the parental, or even grandparental, experience of pathogen infection and/or immune challenge can generate a relative increase in offspring fitness, survival, and immune function (Ben‐Ami et al, 2020 ; Moret, 2006 ; Nystrand & Dowling, 2014 ; Tidbury et al, 2011 ). Less well established is the degree to which parental exposure and intergenerational immune priming carries costs for the recipient offspring (Contreras‐Garduño et al, 2014 ; Leponiemi et al, 2021 ; Zanchi et al, 2011 ). In some cases, costs become evident when the pathogenic environments of parents and offspring are mismatched (reviewed in Roth et al, 2018 ).…”

“…Less well established is the degree to which parental exposure and intergenerational immune priming carries costs for the recipient offspring (Contreras-Garduño et al, 2014;Leponiemi et al, 2021;Zanchi et al, 2011). In some cases, costs become evident when the pathogenic environments of parents and offspring are mismatched (reviewed in Roth et al, 2018).…”