Fruit flies (Tephritidae) are a diverse group of phytophagous species of which the vast majority develop in ripe fruit, causing considerable economic damage to a wide variety of crops. Commonly, flies associate with free living, rot-inducing bacteria (mainly Enterobacteriaceae) which are inoculated into the fruit by ovipositing females. The olive fly (Bactrocera oleae) – a notorious pest of olives, represents a striking exception to this paradigm. Contrary to other frugivorous tephritids, olive flies associate with a single, vertically transmitted bacterium (Candidatus Erwinia dacicola; Enterobacteriaceae), and develop in unripe olives.
We examined the tripartite interaction between larvae, bacteria and fruit ontogeny, hypothesizing that larval dependency on bacteria will change according to the phenology of fruit defensive chemistry. We demonstrate that larvae require their natural complement of bacteria in order to develop in unripe olives. Conversely, when feeding on ripe fruit development proceeds independently of these bacteria. Our experiments suggest that bacteria counteract the inhibitory effect of oleuropein - an active component in green but not in ripe olives, which leads to a decrease the nutritive value of the fruit`s protein.
We suggest that the unique symbiosis in olive flies, compared to other frugivorous Tephritids is understood by considering the interrelationship between the fly, bacteria and host chemistry. When applied in an evolutionary context, this approach may also point out the forces which shaped the attributes of symbiosis across the Tephritidae.
