Change in virus composition before and after field exposure
We show that the bumble bee colonies were initially mainly infected with either honey bee viruses (DWV-B and BQCV) or the bumble bee virus BcDV, while after field exposure bumble bee viruses (CBV and MV 1) joined the group of the most prevalent viruses in the new virome composition. DWV-B, initially highly prevalent in the colonies, could not be detected in the study colonies after field exposure. This result was unexpected as DWV is regarded as an emerging infectious disease commonly responsible for the elevated viral loads found in honey bees (the reservoir host, Tehel et al. 2020) and it is assumed the spill-over of this virus may negatively impact wild bee species . However, the lower prevalence detected after field exposure could be related to bumble bees being inefficient hosts for DWV. Tehel et al. 2020 showed, under laboratory conditions, that the inoculation of DWV by injection produces lower viral replication in B. terrestris than in honey bees, even though bumble bees are bigger in body size. Moreover, B. terrestris showed considerable resistance to DWV infection when fed orally (Gusachenko et al. 2020). Since the oral-fecal route is the main virus transmission route between bees , limited oral transmission would contribute against the quick distribution of this virus among the colonies and may help to explain the low DWV prevalence in our experimental colonies. However, corresponding to the seasonal peak of Varroa destructor mites in honey bee colonies, the spill-over of DWV from managed honey bees can be expected to peak in late summer (, which is after the bumble bee colonies were exposed to the field.
In contrast, viruses related to bumble bees (BcDV, CBV and MV 1) were largely prevalent after field exposure. Those viruses have been reported in several bumble bee species such as Bombus cryptarum , B. terrestris , B. pratorum , and B. pascuorum suggesting their close association with the taxon. Within a host, viruses are in competition with each other. Better adapted viruses should outcompete their counterparts and establish themselves , which could explain the observed shift towards bumblebee associated viruses. This indicates that these viruses might be well adapted to bumble bee hosts rendering them transmission advantages. However, more studies are necessary to determine the true host range of those viruses. In general, the decreasing trends in prevalence and viral loads of honey bee associated viruses suggests that, in contrast to previous claims, virus host shifts from managed honey bees to bumble bee colonies may often have limited impact on the latter under field conditions. However, the current study was not designed to address carry over-effects. The production of new queens and drones, as well as hibernation and colony initiation success of gyns, were not assessed and thus long-term impacts on populations cannot be excluded.
Notably, the virus infections were mostly inconsequential to the performance or health of the colonies. The number of workers, queens, brood cells and hatched pupal cells, as well as weight gain, important colony development parameters that serve as proxies for fitness, remained unaffected. Interestingly, elevated initial DWV-B loads were associated with heightened rates of moth parasitism, whereas higher initial BcDV loads coincided with decreased moth infection rates. Hence, our results remain inconclusive regarding whether virus infections modulate susceptibility for other parasites in bumble bees. As a result of parasite-induced immunosuppression reducing the immune capacity of a host organism, co-infections may be beneficial to one or multiple parasites, facilitating subsequent infections . Conversely, interactions may be antagonistic to at least one of the parasites due to resource competition or cross-effective immune responses . These findings highlight the challenges of comprehending multi-species interactions and underscore the possibility of incorrect risk assessment when investigating parasite impacts in isolation, rather than considering the broader context of pathogen communities .