Heritability estimates of the novel trait ‘suppressed in ovo virus infection’ in honey bees (Apis mellifera)

Abstract

Honey bees are under pressure due to abnormal high colony death rates, especially during the winter. the infestation by the Varroa destructor mite and the viruses that this ectoparasite transmits are generally considered as the bees' most important biological threats. Almost all efforts to remedy this dual infection have so far focused on the control of the Varroa mite alone and not on the viruses it transmits. In the present study, the sanitary control of breeding queens was conducted on eggs taken from drone brood for 4 consecutive years (2015-2018). The screening was performed on the sideline of an ongoing breeding program, which allowed us to estimate the heritabilities of the virus status of the eggs. We used the term 'suppressed in ovo virus infection' (SOV) for this novel trait and found moderate heritabilities for the presence of several viruses simultaneously and for the presence of single viral species. Colonies that expressed the SOV trait seemed to be more resilient to virus infections as a whole with fewer and less severe Deformed wing virus infections in most developmental stages, especially in the male caste. The implementation of this novel trait into breeding programs is recommended. The economic value of the honey bee can be almost entirely attributed to its pollination services for agricultural crops 1. However, honey bees are under pressure due to abnormal high colony death rates, especially during the winter 2. There are several possible explanations for the increased mortality, but the infestation by the Varroa destructor mite and the viruses that this ectoparasite transmits are generally considered the most important biotic threats 3,4. The mite was found to be an efficient vector of viruses even to the extent that initially the clinical symptoms caused by the Deformed wing virus (DWV) were wrongly attributed to the mite 5. The Varroa mite and DWV interact in many different ways, resulting in an increase in DWV virulence 6,7 and colony mortality 8-12. These effects are partially due to the mutualistic symbiotic relationship between both, in which the mite provides transmission of the virus when it feeds on the bee, whereas the virus undermines the immunity of the honey bee by interfering with NF-κB signaling, possibly facilitating the mite's trophic activity 13. Almost all efforts to remedy this dual infection have so far focused on the control of the Varroa mite alone. Indeed, several mitecontrol strategies have been set up in beekeeping practice that rely on acaricide medication or other treatments, biotechnical apicultural methods and selection for Varroa resistance 14. The control of the viruses transmitted by the mite is therefore achieved almost exclusively indirectly, by limiting the severity of the mite infestation. One exception to this is the treatment with double-stranded RNA to provoke a targeted antiviral immune response based on RNA interference, but this is rarely used in beekeeping practice 15,16. The transmission of viruses between bees by the vectoring Varroa mite is descr...

Comparing Survival of Israeli Acute Paralysis Virus Infection among Stocks of U.S. Honey Bees

“…In the absence of significant effects of resident viruses and other confounding factors, our IAPV-inoculated worker survival differences among and within stocks can be interpreted as genetic differences in IAPV susceptibility, which has also been reported in the egg stage [ 25 ]. We chose 3–5 day-old workers to conduct our experiments in workers with a fully-developed immune system because newly-emerged individuals have been shown to be particularly susceptible to disease [ 72 ].…”

“…However, it also can cause sublethal infections [ 21 , 22 ] and persists asymptomatically at low quantities in honey populations, although it is far from ubiquitous [ 18 , 19 ]. Even though RNA interference (RNAi)-based vaccines against IAPV and other viruses are under development [ 23 , 24 ], selectively improving the existing honey bee immune defenses presents a practical and sustainable solution for improving honey bee health [ 25 ].…”

Breeding for Virus Resistance and Its Effects on Deformed Wing Virus Infection Patterns in Honey Bee Queens

“…This trait is described by the absence of virus infections in 10 pooled drone eggs and was the first study to show that the potential of honey bees to suppress virus infections is heritable (R ≈ 0.25). In addition, colonies headed by a SOV-positive queen have fewer and less severe DWV infections in almost all developmental phases of both worker bees and drones [27] indicating the beneficial implications for the health status of the colony. The underlying mechanisms of the SOV trait are yet to be discovered; possible hypotheses could be an increase in the expression [30] or effectivity [17] of the RNA interference pathway, transgenerational effects [31] or increased expression levels of Toll-6 which has been linked with survival after artificial infection with Israeli acute paralysis virus (IAPV) [32].…”

“…As the sole responsible for egg laying, honey bee queens play an important role in vertical transmission. This is reflected by the high presence of DWV encountered in the reproductive tissues, ovaries, spermatheca, and eggs, [23][24][25][26][27] which may be an adaptation to enhance vertical transmission [22]. Transmission from the queen's ovaries to her eggs occurs predominantly by virus particles adhering to the surface of the eggs (transovum) [22].…”

“…In 2012, Belgian beekeepers started screening breeding queens for the presence of viruses in eggs deposited in worker brood cells and found 75% to be infected with at least one virus and 40% to be infected with DWV [26]. These high results led to the start of a yearly sanitary control of the breeding queens and eventually to the discovery of the 'Suppressed in ovo virus infection' trait (SOV) [27]. This trait is described by the absence of virus infections in 10 pooled drone eggs and was the first study to show that the potential of honey bees to suppress virus infections is heritable (R ≈ 0.25).…”