Taxonomy, Diet, and Developmental Stage Contribute to the Structuring of Gut-Associated Bacterial Communities in Tephritid Pest Species

Abstract

Insect-symbiont interactions are receiving much attention in the last years. Symbiotic communities have been found to influence a variety of parameters regarding their host physiology and fitness. Gut symbiotic communities can be dynamic, changing through time and developmental stage. Whether these changes represent real differential needs and preferential relationships has not been addressed yet. In this study, we characterized the structure of symbiotic communities of five laboratory populations that represent five Tephritidae species that are targets for pest control management through the sterile insect technique (SIT), namely Bactrocera oleae, Anastrepha grandis, Anastrepha ludens , and two morphotypes of Anastrepha fraterculus (sp.1 and the Andean lineage). These populations are under artificial or semi artificial rearing conditions and their characterization was performed for different developmental stages and age. Our results demonstrate the presence of a symbiotic community comprising mainly from different Enterobacteriaceae genera. These communities are dynamic across developmental stages, although not highly variable, and appear to have a species-specific profile. Additional factors may contribute to the observed structuring, including diet, rearing practices, and the degree of domestication. Comparison of these results with those derived from natural populations could shed light to changes occurring in the symbiotic level during domestication of Tephritidae populations. Further studies will elucidate whether the changes are associated with modification of the behavior in laboratory strains and assess their effects in the quality of the mass rearing insects. This could be beneficial for improving environmentally friendly, species-specific, pest control methods, such as the SIT.

Comparative Microbiomics of Tephritid Frugivorous Pests (Diptera: Tephritidae) From the Field: A Tale of High Variability Across and Within Species

“…Differences between microbiome profiles can be related to life history traits and environmental factors including life stage ( Lauzon et al, 2009 ; Andongma et al, 2015 ), diet ( Santo Domingo et al, 1998 ; De Vries et al, 2004 ; Colman et al, 2012 ; Morrow et al, 2015 ), or technical artifacts ( De Cock et al, 2019 ). Consistent with what has been reported in other studies on frugivorous tephritids ( Thaochan et al, 2010 ; Wang et al, 2011 ; Andongma et al, 2015 ; Morrow et al, 2015 ; Augustinos et al, 2019 ), the gut microbiome profiles of third instar larvae of the ten fruit fly species targeted by the present study were mainly composed of Proteobacteria and Firmicutes which together represented more than 98.49% of reads in all tephritid species targeted. Andongma et al (2015) suggested that Proteobacteria might be the most abundant phylum in earlier developmental stages of Bactrocera , while Firmicutes the most abundant in adult stages, possibly as a result of changes in habitat and diet.…”

“…Most of the currently available research on tephritid gut microbiomics focuses on fruit fly laboratory populations (i.e., fed with artificial diets) and often aims at investigating the optimal rearing conditions for species of interest for the sterile insect technique (SIT) ( Augustinos et al, 2015 , 2019 ; Kyritsis et al, 2017 , 2019 ; Asimakis et al, 2019 ) while the composition and levels of variability of microbiome profiles of wild tephritid flies are far less known.…”

Manipulation of insect gut microbiota towards the improvement of Bactrocera oleae artificial rearing

“…Other less abundant genera such as Enterobacter sp., Providencia sp., Klebsiella sp. (Manousis & Ellar, 1988; Augustinos et al, 2019; Koskinioti et al, 2019), Acetobacter tropicalis (Kounatidis et al, 2009), Pantoea sp. (Ben‐Yosef et al, 2015; Koskinioti et al, 2019), Pseudomonas sp.…”

“…(Blow et al, 2019), and Morganella sp. (Augustinos et al, 2019) have also been identified in the olive fruit fly gut but their role in the fly’s biology is not fully known yet.…”

“…E. dacicola is only essential in natural populations and laboratory strains that feed on olive fruits and is replaced by other transiently acquired bacteria during feeding on artificial diets (Sacchetti et al, 2008). Some of these bacteria, such as Morganella morganii , are potentially pathogenic and might be the reason for B. oleae laboratory rearing inefficiency (Konstantopoulou et al, 2005; Kounatidis et al, 2009; Estes et al, 2011; Augustinos et al, 2019). Re‐introduction of Ca .…”