Abstract

The sterile insect technique (SIT) as an eco‐friendly and reliable strategy has been used to control populations of insect pests of agricultural, veterinary and human health importance. Successful applications of SIT rely on the high‐level ecological fitness of sterile males. A suitable and stable gut microbiome can contribute to the ecological fitness of insect by influencing their physiology, biochemistry and development processes. Here, we show that a shift in the gut bacterial composition and structure by sterilizing irradiation, characterized by a decrease in the major gut microbiota community Enterobacteriaceae, an expansion of the minor members (e.g., Bacillaceae) and a higher richness and diversity, is tightly linked to radiation‐induced ecological fitness (male mating competitiveness, flight capacity, survival rate and life span) decline in Bactrocera dorsalis (Hendel) sterile males. Function prediction of gut microbiota indicated that changes in microbiome taxonomy tend to drive microbiome functional shifts. A higher nutrient consumption of the flourishing minor gut microbiota may cause a decline in nutrients and energy metabolic activity of host and then result in the reduced ecological fitness of irradiated flies. Furthermore, we found that a gut bacterial strain Klebsiella oxytoca (BD177) can restore ecological fitness by improving food intake and increasing haemolymph sugar and amino acid levels of irradiated B. dorsalis flies. Our findings suggest that gut symbiont‐based probiotics can be used as agents for reversing radiation‐induced ecological fitness decrease.

Highlights

  • The sterile insect technique (SIT) has been used for decades to control insect pests of agricultural, veterinary and human health importance (Lees, Gilles, Hendrichs, Vreysen, & Bourtzis, 2015; Leftwich, Bolton, & Chapman, 2016)

  • A crucial issue for the successful and practical implementation of SIT on a large scale is how to produce a large number of high quality sterile males, that can compete with wild males for

  • We first demonstrate that irradiation damage on host ecological fitness was interlinked with intestinal microbial community dysbiosis, using the classic sterile male insect model

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Summary

| INTRODUCTION

The sterile insect technique (SIT) has been used for decades to control insect pests of agricultural, veterinary and human health importance (Lees, Gilles, Hendrichs, Vreysen, & Bourtzis, 2015; Leftwich, Bolton, & Chapman, 2016). The decline of flight performance, female attraction and longevity of irradiated males in Tephritidae pests and mosquitoes has been documented (Helinski, Parker, & Knols, 2009; López-­ Martínez & Hahn, 2014) These negative side effects may be due to radiation exposure that can impose various impacts on an organism, for example direct disruption of atomic structures, and indirect damage to nucleic acids, proteins and lipids by reactive chemical materials generated from the radiolysis of water (Azzam, Jay-­Gerin, & Pain, 2012). SIT may have some limitations related to the ecological fitness of sterile male fruit flies, but manipulation of gut symbionts maybe an alternative strategy for improving the mass rearing efficiency of high-­quality sterile males (Ben Ami et al, 2010). We found that K. oxytoca (BD177) re-­infection improved food intake, sugar and amino acid levels in the haemolymph of irradiated flies and the potential contribution of K. oxytoca (BD177) to repair radiation damage and improvement in the ecological fitness of sterile males

| METHODS
| Irradiation procedures
2.10 | Data accessibility
Findings
| DISCUSSION
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