Abstract
We studied the microbiota of a highly polyphagous insect, Anastrepha ludens (Diptera: Tephritidae), developing in six of its hosts, including two ancestral (Casimiroa edulis and C. greggii), three exotic (Mangifera indica cv. Ataulfo, Prunus persica cv. Criollo, and Citrus x aurantium) and one occasional host (Capsicum pubescens cv. Manzano), that is only used when extreme drought conditions limit fruiting by the common hosts. One of the exotic hosts (“criollo” peach) is rife with polyphenols and the occasional host with capsaicinoids exerting high fitness costs on the larvae. We pursued the following questions: (1) How is the microbial composition of the larval food related to the composition of the larval and adult microbiota, and what does this tell us about transience and stability of this species’ gut microbiota? (2) How does metamorphosis affect the adult microbiota? We surveyed the microbiota of the pulp of each host fruit, as well as the gut microbiota of larvae and adult flies and found that the gut of A. ludens larvae lacks a stable microbiota, since it was invariably associated with the composition of the pulp microbiota of the host plant species studied and was also different from the microbiota of adult flies indicating that metamorphosis filters out much of the microbiota present in larvae. The microbiota of adult males and females was similar between them, independent of host plant and was dominated by bacteria within the Enterobacteriaceae. We found that in the case of the “toxic” occasional host C. pubescens the microbiota is enriched in potentially deleterious genera that were much less abundant in the other hosts. In contrast, the pulp of the ancestral host C. edulis is enriched in several bacterial groups that can be beneficial for larval development. We also report for the first time the presence of bacteria within the Arcobacteraceae family in the gut microbiota of A. ludens stemming from C. edulis. Based on our findings, we conclude that changes in the food-associated microbiota dictate major changes in the larval microbiota, suggesting that most larval gut microbiota is originated from the food.
Highlights
The critical role the microbiome plays in supporting or outright regulating key metabolic pathways in organisms including humans or in dealing with emerging environmental challenges is being unraveled at an unprecedented speed (Gevers et al, 2012; Gilbert et al, 2014; Bauer et al, 2020; Ayyasamy et al, 2021; Schmidt and Engel, 2021)
We found that the composition of the gut microbiota of A. ludens larvae is plastic rather than stable, depending largely on the microbiota associated with the pulp on which they fed
We found that the gut microbiota of A. ludens is unstable and that its composition and richness depend on the microbiota associated with the particular plant the larvae of this highly polyphagous species fed on
Summary
The critical role the microbiome plays in supporting or outright regulating key metabolic pathways in organisms including humans or in dealing with emerging environmental challenges is being unraveled at an unprecedented speed (Gevers et al, 2012; Gilbert et al, 2014; Bauer et al, 2020; Ayyasamy et al, 2021; Schmidt and Engel, 2021). In contrast to resident microbiota, the transient microbiota is exclusively acquired from the environment and usually passes through the gut and is expelled via the feces. It is not capable of establishing itself permanently, since its rate of loss exceeds its rate of permanence (Erkosar and Leulier, 2014; Derrien and van Hylckama Vlieg, 2015; Ma and Leulier, 2018; Hammer et al, 2019)
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