Knock‐on community impacts of a novel vector: spillover of emerging DWV‐B from Varroa‐infested honeybees to wild bumblebees

Abstract

Novel transmission routes can directly impact the evolutionary ecology of infectious diseases, with potentially dramatic effect on host populations and knock‐on effects on the wider host community. The invasion of Varroa destructor, an ectoparasitic viral vector in Western honeybees, provides a unique opportunity to examine how a novel vector affects disease epidemiology in a host community. This specialist honeybee mite vectors deformed wing virus (DWV), an important re‐emerging honeybee pathogen that also infects wild bumblebees. Comparing island honeybee and wild bumblebee populations with and without V. destructor, we show that V. destructor drives DWV prevalence and titre in honeybees and sympatric bumblebees. Viral genotypes are shared across hosts, with the potentially more virulent DWV‐B overtaking DWV‐A in prevalence in a current epidemic. This demonstrates disease emergence across a host community driven by the acquisition of a specialist novel transmission route in one host, with dramatic community level knock‐on effects.

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

“…We collected foraging bees (355 A. mellifera, 281 Bombus pascuorum, 640 B. terrestris and 38 Bombus lucorum individuals) within a 1 × 1 km area as described in detail in (Manley et al, 2019), from four Varroafree islands; three Varroa-positive islands; and five Varroa-positive mainland sites ( Figure S1, Table S1). We differentiated between B. terrestris and B. lucorum via a mtDNA length polymorphism (Table S2).…”

“…We differentiated between B. terrestris and B. lucorum via a mtDNA length polymorphism (Table S2). We extracted DNA from homogenised gut tissue using Chelex following the manufacturer's instructions, and RNA using Trizol and bromo-chloropropane from individuals (gut homogenate and half the head and thorax (bisected laterally)) as described in detail in Manley et al (2019). RNA was resuspended in 100 μl (A. mellifera) or 400 μl (Bombus species) of nuclease-free water.…”

“…We used RStudio (v0.99.896) for all statistical analyses. In the full models we included three-way interaction between fixed effects; Varroa-presence/absence, species (a factor with three levels: A. mellifera, B. terrestris and B. pascuorum) and island/ mainland location; latitude and sunshine hours duration were included as proxies for favourable disease transmission as additional fixed effects (Fürst et al, 2014;Manley et al, 2019): field site and individual were included as random effects (individual was added to account for over-dispersion in the models [Harrison, 2014]). To test if BQCV and SBPV prevalence was affected by Varroa-presence we ran generalised linear mixed models (GLMMs) lme4 package (v1.1-12) (Bates, Maechler, Bolker, & Walker, 2015) with binomial error distribution and logit link function.…”

“…Pollinators are host to a large number of RNA viruses that are known to be pathogenic to honeybees, but have more recently been identified as multihost pathogens, prevalent in wild bee populations (Evison et al, 2012;Fürst, McMahon, Osborne, Paxton, & Brown, 2014;Levitt et al, 2013;Manley, Boots, & Wilfert, 2015;Manley et al, 2019;McMahon et al, 2015;Singh et al, 2010). There are known differences in viral prevalence and viral load across honeybee and bumblebee hosts for many RNA viruses (McMahon et al, 2015).…”

“…Deformed wing virus potentially increases in the mite by replication (Gisder, Aumeier, & Genersch, 2009;Ryabov et al, 2014), or possibly through bioaccumulation of virus particles through blood feeding (Erban et al, 2015). While V. destructor is a specialist vector restricted to honeybees, it indirectly increases DWV prevalence and titre in sympatric bumblebees by dramatically increasing the transmission potential of A. mellifera (Manley et al, 2019), i.e., A. mellifera becomes a "superspreader" host species (Lloyd-Smith, Schreiber, Kopp, & Getz, 2005;Manley et al, 2019).…”