Symbiotic bacteria enable olive fly larvae to overcome host defences.

Michael Ben-Yosef,Zohar Pasternak,Boaz Yuval,Edouard Jurkevitch

doi:10.1098/rsos.150170

Abstract

Ripe fruit offer readily available nutrients for many animals, including fruit fly larvae (Diptera: Tephritidae) and their associated rot-inducing bacteria. Yet, during most of their ontogeny, fruit remain chemically defended and effectively suppress herbivores and pathogens by high levels of secondary metabolites. Olive flies (Bactrocera oleae) are uniquely able to develop in unripe olives. Unlike other frugivorous tephritids, the larvae maintain bacteria confined within their midgut caeca. We examined the interaction between larvae, their associated bacteria, and fruit chemical defence, hypothesizing that bacterial contribution to larval development is contingent on the phenology of fruit defensive chemistry. We demonstrate that larvae require their natural complement of bacteria (Candidatus Erwinia dacicola: Enterobacteriaceae) in order to develop in unripe olives. Conversely, when feeding on ripe fruit, larval development proceeds independently of these bacteria. Our experiments suggest that bacteria counteract the inhibitory effect of oleuropein—the principal phenolic glycoside in unripe olives. In light of these results, we suggest that the unique symbiosis in olive flies, compared with other frugivorous tephritids, is understood by considering the relationship between the fly, bacteria and fruit chemistry. When applied in an evolutionary context, this approach may also point out the forces which shaped symbioses across the Tephritidae.

Highlights

Fruits undergo extensive transformations during their ripening process, before maturing into a fleshy, energy-rich reward for seed dispersers [1,2]
We examined the interaction between olive fly larvae, their symbiotic bacteria and olive fruit chemistry
Treating females with antibiotics had no effect on egg viability and resulted in aposymbiotic larvae which actively fed during the experiments but failed to develop in unripe fruit

Summary

Introduction

Fruits undergo extensive transformations during their ripening process, before maturing into a fleshy, energy-rich reward for seed dispersers [1,2]. Unripe fruit usually offer little nutrition and are resistant to attack by herbivores and pathogens due. To high contents of secondary metabolites with anti-nutritive, antimicrobial, deterrent and toxic effects, 2 securing a safe environment for the seeds to mature The fate of secondary metabolites during the ripening process is usually to be neutralized or degraded [3,4,5]. Together with the build-up of fruit sugar content, decrease in acidity and softening of tissues which are generally observed during ripening, these processes eventually contribute to the high nutritional value of mature fruit [1]. The ecological consequence of this adaptive schedule for herbivores and microbes is that unripe fruit are usually off the menu

Methods

Results

Discussion

Conclusion