Experimental viral spillover can harmBombus terrestrisworkers under field conditions

Abstract

1. Deformed wing virus (DWV), notorious for its virulence in the western honey bee (Apis mellifera) when vectored by the ectoparasitic mite Varroa destructor, is also widespread among wild bumble bee species, presumably through spillover from honey bees. Experimental studies on the virulence of DWV in Bombus spp. have provided equivocal results and have until now been confined to bumble bees under laboratory conditions.2. Here, we inoculated commercially reared Bombus terrestris workers with DWV-A through feeding or injection and introduced them into experimental colonies placed in the field, thus exposing them to the environment and associated stressors. We monitored the survival of inoculated worker bumble bees and quantified their viral load at 10 days post inoculation.3. Bombus terrestris workers injected with DWV-A supported high viral loads and exhibited significantly reduced median survival compared to controls. Bumble bees inoculated by feeding had low or zero detectable viral loads while their mortality did not differ from the control group. 4. Our results demonstrate that, although DWV-A is pathogenic for commercial B. terrestris, the risks for individual fitness from spillover of DWV-A during foraging on shared flowers appear limited.

Host Barriers Limit Viral Spread in a Spillover Host: A Study of Deformed Wing Virus in the Bumblebee Bombus terrestris

“…In support of this view, when inoculated orally, a likely more natural mode of infection of bumblebees in the field [ 9 , 18 ], we also found that B. terrestris shed less DWV in faeces than did A. mellifera . Our data on viral shedding, along with the overall lower total DWV titres accumulating in adult B. terrestris compared to A. mellifera [ 28 , 29 ] and the lower infection rate observed after an oral challenge [ 27 ], suggest that B. terrestris constitutes a less suitable host for DWV-B than A. mellifera . Thus, DWV’s epidemiology in multi-species communities of bees is likely driven primarily by spillover from A. mellifera [ 10 , 11 , 12 ], the presumed reservoir host of this virus, rather than onward transmission from infected B. terrestris .…”

“…In comparison, DWV has been shown to replicate in various tissue types of A. mellifera [42][43][44]. Furthermore, even though B. terrestris is known to support replication of DWV, shown by increasing virus titres after experimental infection [27][28][29]31], the low virus shedding we observed here in infected B. terrestris might additionally indicate a lack of molecular compatibility between DWV and B. terrestris, e.g., that the needed enzymes for virus release from the host cell are insufficient. For example, avian influenza virus spilling over to humans is often characterised by a viral neuraminidase that is insufficient to cleave the viral progeny from human host proteins, thus hindering effective cell release of new virions and viral spread despite virus replication [45].…”

“…For example, when varroa carries DWV and transmits it by biting directly into the haemocoel of a pupa or adult A. mellifera , DWV effectively circumvents the honeybee’s gut barrier and replicates rapidly to a high titer and elevated virulence [ 8 , 26 ]. In a similar way, investigation of the bumblebee spillover host Bombus terrestris has shown that the experimental mode of transmission, i.e., oral versus vector-based transmission directly into the haemocoel, is a determinant of the disease severity of DWV infecting B. terrestris [ 27 , 28 ], as it is for A. mellifera , albeit with lower overall virulence in B. terrestris . These studies suggest that DWV is less successful at establishing an infection in B. terrestris when transmitted orally versus by injection, potentially due to within-host (gut) barriers that restrict DWV’s spread through the host body.…”

Endosymbionts that threaten commercially raised and wild bumble bees (Bombus spp.)

“…Few experiments have addressed the incidence of disease in DWV-infected bumble bees, but DWV has been shown to increase mortality in experimentally infected individuals both alone and with co-infection with the protozoan Apicystis bombi (Fürst et al 2014;Graystock et al 2016). Although a laboratory study considering the efficacy of proposed natural transmission routes suggested that transmission in the wild may be limited (Gusachenko et al 2020;Streicher et al 2023), research has demonstrated spillover from honey bees to bumble bees (Tehel et al 2022) and a potential introduction with non-native bumble bees (Arbetman et al 2013). The closely related Varroa destructor viruses (VDVs) and kakugo virus (KV) are considered by some to be variants of a DWV species complex (McMahon et al 2015).…”