Friend or Foe: Establishing the role of Arsenophonus in honey bee health

Georgia Drew, University of Liverpool

Supervised by Greg Hurst & Alistair Darby (UoL), Giles Budge, Kat Roberts, Kirsty Stainton (FERA)


Endosymbiotic bacteria of the genus Arsenophonus form associations with a diverse range of arthropod hosts.  These symbiotic interactions are varied, ranging from reproductive parasites to coevolving obligate mutualists, and the predominant mode of symbiont transmission within the clade is vertical. Previous metagenomic studies indicate that Arsenophonus forms associations with the European honey bee, Apis mellifera. Despite the evolutionary and ecological significance of Apis mellifera and the potentially important impacts of Arsenophonus on Apis biology, interactions between these players have remained uncharacterised. This thesis reports Arsenophonus is common within UK populations of A. mellifera and the genetic diversity of circulating strains appears to be low. Phylogenomic analysis confirms the position of the symbiont within the genus Arsenophonus, most closely related to the male-killer strain associated with the parasitoid wasp, Nasonia vitripennis. Epidemiological patterns are detected, with Arsenophonus occurrence varying over space and time. Spatial variation is evident at local scales but infection prevalence remains uniform with larger geography. Conserved seasonal dynamics, with prevalence low in spring and increasing into autumn, hint at the role of an environmental reservoir driving infection dynamics and argue against vertical transmission. The low prevalence of Arsenophonus among solitary Colletes spp. suggests spill over risk is low and associations are uncommon, perhaps mediated by the fixation of another endosymbiont, Wolbachia, in solitary Anthophila populations. FISH analysis indicates Arsenophonus is localised within the A. mellifera gut and forms diffuse infections, however associations are highly dynamic. Infections can be lost rapidly under both field and laboratory conditions and correlate with reduced exposure to the environment. Absence in spring samples, in eggs, larvae and newly emerged workers argues against direct vertical transmission of Arsenophonus in A. mellifera, contrasting markedly with other Arsenophonus-host interactions examined to date. Horizontal transmission via social interactions can occur, but with variable success, possibly influenced by super spreader or stochastic effects. Multiple lines of evidence suggest environmental exposure is key to infection maintenance and social transmission may further drive the dissemination of Arsenophonus within a colony. These findings demonstrate evolutionary lability within this common clade of insect symbionts and have repercussions for studying transitions in symbiotic lifestyle.

Transitions in Symbiosis: Evidence for Environmental Acquisition & Social Transmission within a Clade of Heritable Symbionts