Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees

Abstract

Typically, pathogens infect multiple host species. Such multihost pathogens can show considerable variation in their degree of infection and transmission specificity, which has important implications for potential disease emergence. Transmission of multihost pathogens can be driven by key host species and changes in such transmission networks can lead to disease emergence. We study two viruses that show contrasting patterns of prevalence and specificity in managed honeybees and wild bumblebees, black queen cell virus (BQCV) and slow bee paralysis virus (SBPV), in the context of the novel transmission route provided by the virus‐vectoring Varroa destructor. Our key result is that viral communities and RNA virus genetic variation are structured by location, not host species or V. destructor presence. Interspecific transmission is pervasive with the same viral variants circulating between pollinator hosts in each location; yet, we found virus‐specific host differences in prevalence and viral load. Importantly, V. destructor presence increases the prevalence in honeybees and, indirectly, in wild bumblebees, but in contrast to its impact on deformed wing virus (DWV), BQCV and SBPV viral loads are not increased by Varroa presence, and do not show genetic evidence of recent emergence. Effective control of Varroa in managed honeybee colonies is necessary to mitigate further disease emergence, and alleviate disease pressure on our vital wild bee populations. More generally, our results highlight the over‐riding importance of geographical location to the epidemiological outcome despite the complexity of multihost‐parasite interactions.

Genetic Strain Diversity of Multi-Host RNA Viruses that Infect a Wide Range of Pollinators and Associates is Shaped by Geographic Origins

“…The presence of apiaries has shown to cause a high prevalence of DWV and BQCV in wild pollinators [19] and species associated with beehives [10,13,64]. We found BQCV in honey bees but no other pollinator, which may be due to the higher BQCV prevalence in honey bees compared to other bees [65], and the low number of wild bee pollinators in our sample set. We only detected DWV in Argentine ants from apiaries, which could indicate that ants acquire the virus from bees, potentially by scavenging in apiaries.…”

“…To understand the current epidemic of bee viruses, it is key to determine the role of the host species and geographic distribution [12,65]. By placing the sequences generated in this study within a global phylogeny, we found that both KBV and DWV showed strong grouping by geographic regions.…”

Predictors of virus prevalence and diversity across a wild bumblebee community

“…Another possibility is that both viruses circulate in the population, but infection with one causes damage to the host in such a way that susceptibility to the second is dramatically increased, perhaps in a manner analogous to HIV's synergism with TB though immune suppression (Kwan & Ernst, 2011) or influenza virus' changing of the environment of the nasopharynx, allowing secondary bacterial invasion (Joseph et al, 2013). Viral coinfections are ubiquitously reported in prevalence studies in bees (Anderson & Gibbs, 1988;Bacandritsos et al, 2010;Blažytė-Čereškienė et al, 2016;Chen et al, 2004;Choe et al, 2012;Evans, 2001;Gajger et al, 2014;Manley et al, 2020;McMahon et al, 2015;Mouret et al, 2013;Nielsen et al, 2008;Roberts et al, 2017;Thu et al, 2016), but to our knowledge, only McMahon et al (2015) and Manley et al (Manley et al, 2020) tested for a departure from random expectations of infection, and no departure was found. However, non-random associations between parasites appear common, having been reported in, among other taxa including mammals (Behnke et al, 2005;Griffiths et al, 2011;Jolles et al, 2008), birds (Clark et al, 2016), arthropods (Hajek & van Nouhuys, 2016;Václav et al, 2011) and plants (Biddle et al, 2012;Seabloom et al, 2009).…”

“…Bumblebee-limited viruses necessarily undergo multiple independent bottlenecking events when the viruses can only survive in overwintering queens, potentially maintaining diversity through reduced selection efficiency. This would initially seem to apply to SBPV, as McMahon et al (2015) and Manley et al (2020) report that SBPV is often found at higher prevalences in bumblebees than in sympatric honeybees during in summer. However, over winter, bumblebee populations are reduced to individual queens while honeybee colonies are maintained at population sizes in the thousands.…”

“…Another possibility is that both viruses circulate in the population, but infection with one causes damage to the host in such a way that susceptibility to the second is dramatically increased, perhaps in a manner analogous to HIV's synergism with TB though immune suppression (Kwan & Ernst, 2011) or influenza virus' changing of the environment of the nasopharynx, allowing secondary bacterial invasion (Joseph et al, 2013). Viral coinfections are ubiquitously reported in prevalence studies in bees (Anderson & Gibbs, 1988;Bacandritsos et al, 2010;Blažytė-Čereškienė et al, 2016;Chen et al, 2004;Choe et al, 2012;Evans, 2001;Gajger et al, 2014;Manley et al, 2020;McMahon et al, 2015;Mouret et al, 2013;Nielsen et al, 2008;Roberts et al, 2017;Thu et al, 2016), but to our knowledge,…”