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 .