Rapid spread of nutritional Wolbachia symbionts across and within solitary bee species

Abstract

Maternally inherited, intracellular Bacteria of the genus Wolbachia are extremely widespread among arthropods. Their evolutionary success is owed to frequent host shifts and rapid subsequent spread within host populations, often facilitated by Wolbachia-induced reproductive manipulations. Theory suggests that carrying Wolbachia must also be beneficial for a successful spread, however the nature of such benefits remains unclear. Here, we demonstrate that Wolbachias success in many solitary bee species is strongly associated with the presence of a gene cassette enabling Wolbachia to synthesize Biotin (vitamin B7). This ability is absent from almost all other Wolbachia strains but common among bee associated strains. We show that Wolbachia occurs in up to 70% of all bee species and that strains carrying this rare genomic element have independently spread into numerous bee hosts recently. We further demonstrate that the presence of the biotin operon is associated with specialised diets in several bee species, suggesting a previously overlooked nutritional role of Wolbachia in this group of important pollinators. Overall, our results suggest that nutritional benefits provided by symbionts may represent a more widespread and important mechanism by which reproductive manipulators spread into new host species than previously appreciated.