Dynamics of the Queensland Fruit Fly Microbiome through the Transition from Nature to an Established Laboratory Colony

Abstract

The transition from nature to laboratory or mass rearing can impose significant physiological and evolutionary impact on insects. The Queensland fruit fly (also known as ‘Qfly’), Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), is a serious economic pest that presents major challenges for horticulture industries in Australia. The sterile insect technique (SIT) is being developed to manage outbreaks in regions that remain free of Qfly and to suppress populations in regions where this species is endemic. The biology of Qfly is intimately connected to its microbiome. Therefore, changes in the microbiome that occur through domestication have implications for SIT. There are numerous studies of the microbiome in Qfly larvae and adults, but there is little information on how the microbiome changes as Qfly laboratory colonies are established. In this study, high-throughput Illumina sequencing was used to assess the Qfly microbiome in colonies reared from wild larvae, collected from fruit, for five generations, on a gel-based larval diet. Beta diversity analysis showed that the bacterial communities from Generation 5 (G5) clustered separately from earlier generations. At the genus level, bacterial communities were significantly different between the generations and mostly altered at G5. However, communities were found similar at phyla to family taxonomic levels. We observed high abundance of Morganella and Burkholderia at the genus level in the larval and pupal stages respectively at G5, but these were not detected in earlier generations. Overall, our findings demonstrate that the domestication process strongly affects the Qfly microbiome and prompts questions about the functional relationship between the Qfly and its microbiome, as well as implications for the performance of insects that have been domesticated and mass-reared for SIT programs.

Eating eggplants as a cucurbit feeder: Dietary shifts affect the gut microbiome of the melon fly Zeugodacus cucurbitae (Diptera, Tephritidae)

“…Moreover, changes in the larval microbiome due to captivity can occur in even relatively short periods. Majumder et al (2022), for example, already detected changes in larval microbiomes after a single generation in captivity. Interestingly, changes in the adult microbiome took more generations before they started to occur.…”

Dynamics of the Gut Bacteriome During a Laboratory Adaptation Process of the Mediterranean Fruit Fly, Ceratitis capitata

“…This finding was in line with previous studies performed on C. capitata populations (Aharon et al, 2013 ; Malacrinò et al, 2018 ). To the best of our knowledge, the effect of laboratory adaptation was investigated only in two tephritid flies: Anastrepha fraterculus (Salgueiro et al, 2020 ) and Bactrocera tryoni (Majumder et al, 2022 ). Both studies using 16S rRNA gene amplicon data sets reported a strong effect of the degree of laboratory adaptation on the structure of the gut bacterial community at each developmental stage.…”

“…However, the colonization and production methods that may lead to the production of flies with improved fitness, are indeed very challenging. The laboratory adaptation processes of the strains used under artificial mass rearing have been reported to improve development, survival, and reproduction under a laboratory environment (Liedo et al, 2007 ; Diamantidis et al, 2011 ; Majumder et al, 2022 ), but at the same time, they commonly have detrimental effects on field performance (Liedo et al, 2007 ; Pereira et al, 2007 ; Hernández et al, 2009 ). The culturing of tephritid fruit flies is generally associated with fast development of flies, increase in body size, and survival while some incompatibility with wild flies may evolve in mating behavior and reduced environmental tolerance (Mangan, 1997 ; Miyatake, 1998 ; Briceño and Eberhard, 2002 ; Zygouridis et al, 2014 ; Schutze et al, 2015 ; Pérez et al, 2018 ).…”

“…The family, Enterobacteriaceae has been reported as the main component of the core microbiome of wild larvae of various tephritid flies (De Cock et al, 2020 ) and wild adults of Zeugodacus cucurbitae (Yong et al, 2019 ). In terms of abundance and despite the variability between studies (including strain, geographical locations, developmental stage, and rearing conditions), members of the family, Enterobacteriaceae have been reported to represent the major component of laboratory and wild tephritid populations, with Klebsiella, Citrobacter, Enterobacter, Providencia, Proteus , and Bacillus repeatedly detected in different species of fruit flies, including C. capitata (Behar et al, 2008c ; Malacrinò, 2018 ; Nikolouli et al, 2020 ), Bactrocera dorsalis (Yong et al, 2017 ; Zhao et al, 2018 ), Bactrocera tryoni (Woruba et al, 2019 ; Majumder et al, 2022 ), Bactrocera oleae (Ben-Yosef et al, 2015b ; Bigiotti et al, 2021 ), Zeugodacus cucurbitae (Hadapad et al, 2016 ; Asimakis et al, 2019 ; Yong et al, 2019 ), and Anastrepha fraterculus (Augustinos et al, 2019 ; Salgueiro et al, 2020 ). Moreover, some tephritid fruit flies also harbor Pseudomonas (Behar et al, 2008c ), Morganella (Salas et al, 2017 ), and Serratia (Fitt and O'Brien, 1985 ) which are often harmless but can be occasional pathogens.…”

Role of gut symbionts of insect pests: A novel target for insect-pest control

“…To decode the functional implications of these gut symbionts, it is necessary to study their distribution. Thus, we have summarized recent metagenomics studies (whole insect and insect gut) of several insect pests which is demonstrated by phylum wise composition of bacteria in Figure 1A ( Yong et al, 2017 ; Tokuda et al, 2018 ; Bozorov et al, 2019 ; Gawande et al, 2019 ; Shah et al, 2020 ; Asimakis et al, 2021 ; Deguenon et al, 2021 ; He et al, 2021 ; Tegtmeier et al, 2021 ; Yu et al, 2021 ; Csorba et al, 2022 ; Li S. et al, 2022 ; Majumder et al, 2022 ; Wang et al, 2022 ). We have noticed with taken examples that Proteobacteria, Firmicutes and Actinobacteria were the most dominant phyla present in the insect gut could be due to their diverse roles in nutrition.…”