Bitter friends are not always toxic: The loss of acetic acid bacteria and the absence of Komagataeibacter in the gut microbiota of the polyphagous fly Anastrepha ludens could inhibit its development in Psidium guajava in contrast to A. striata and A. fraterculus that flourish in this host

Abstract

The gut microbiota is key for the homeostasis of many phytophagous insects, but there are few studies comparing its role on host use by stenophagous or polyphagous frugivores. Guava (Psidium guajava) is a fruit infested in nature by the tephritids Anastrepha striata and A. fraterculus. In contrast, the extremely polyphagous A. ludens infests guava only under artificial conditions, but unlike A. striata and the Mexican A. fraterculus, it infests bitter oranges (Citrus x aurantium). We used these models to analyze whether the gut microbiota could explain the differences in host use observed in these flies. We compared the gut microbiota of the larvae of the three species when they developed in guava and the microbiota of the fruit pulp larvae fed on. We also compared the gut microbiota of A. ludens developing in C. x aurantium with the pulp microbiota of this widely used host. The three flies modified the composition of the host pulp microbiota (i.e., pulp the larvae fed on). We observed a depletion of Acetic Acid Bacteria (AAB) associated with a deleterious phenotype in A. ludens when infesting P. guajava. In contrast, the ability of A. striata and A. fraterculus to infest this fruit is likely associated to a symbiotic interaction with species of the Komagataeibacter genus, which are known to degrade a wide spectrum of tannins and polyphenols. The three flies establish genera specific symbiotic associations with AABs. In the case of A. ludens, the association is with Gluconobacter and Acetobacter, but importantly, it cannot be colonized by Komagataeibacter, a factor likely inhibiting its development in guava.

Insights into the differences related to the resistance mechanisms to the highly toxic fruit Hippomane mancinella (Malpighiales: Euphorbiaceae) between the larvae of the sister species Anastrepha acris and Anastrepha ludens (Diptera: Tephritidae) through comparative transcriptomics

“…, Komagataeibacter ) and a fruit fly (the stenophagous A . striata ) was recently reported ( Ochoa-Sánchez et al, 2022 ). Here we chose as study model another fruit fly species adapted to monophagy: Anastrepha acris Stone (Diptera: Tephritidae), which is phylogenetically very close to A. ludens ( Mengual et al, 2017 ), but exclusively infests fruits of Hippomane mancinella L (Malpighiales: Euphorbiaceae) ( Aluja and Norrbom, 2000 ; Aluja et al, 2020 ).…”

Infestation of Pink-Flesh Guava by Frugivorous Fruit Flies (Diptera: Tephritidae and Lonchaeidae) in an Orchard of Mixed Mandarin and Guava Trees at Morelos, Mexico

“…We suggested pink-flesh guava cultivars were in general more susceptible and better hosts for Anastrepha species. Large guava fruit size, nutritional quality, and thin and smooth peel might enable infestation by Anastrepha spp., Neosilba spp., and Zaprionous indianus Gupta fruit flies (Aluja et al 2014, Lasa et al 2017, Moreira et al 2018, Ochoa et al 2022, Birke unpublished data).…”

“…Feral guavas, in the State of Veracruz, are not naturally infested by A. ludens (Birke and Aluja 2011, Birke et al 2015) but are very susceptible to A. striata in the lowlands, A. fraterculus in the highlands, and occasionally by Anastrepha obliqua (Macquart). Peel firmness, chemical content of feral guavas, and absence of microbiota hinder A. ludens larvae from developing successfully in white-flesh guavas (Birke et al 2015, Ochoa et al 2022). A. striata usually attacks guavas when fruits are small and immature; in contrast, A. fraterculus oviposits in fully developed immature-green fruit (Birke et al 2015).…”

Larval Rearing and Nutrition of the Polyphagous Tephritid Pest Anastrepha ludens on Artificial Diets with Calcium Alginate, Agar, or Carrageenan as Gelling Agents at Various Concentrations and across Extreme Larval Density Conditions

“…Because ammonium is a by-product of protein metabolism by bacteria [75] and uric acid is a by-product of protein metabolism by larvae [76], the changes in the levels of these metabolites caused by calcium alginate in the diets suggests an alteration in protein metabolism, specifically symbiotic nitrogen fixation. Calcium ions adversely affect bacterial nitrogen fixation, as shown in model plant species [77], and symbiotic nitrogen-fixing bacteria species have been reported in tephritids such as Bactrocera dorsalis (Hendel), Ceratitis capitata (Wiedemann), and A. ludens [78][79][80]. However, there is still very little information on the role of the microbiota of Diptera in general and of A. ludens in particular in their digestion processes, nutrient absorption, development, and physical performance [81].…”