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

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.MO-S would like to thank CONACyT for the graduate-school scholarship he received throughout his MSc studies (No. 1800821). This study was principally funded with resources from the Mexican Campaña Nacional Contra Moscas de la Fruta [DGSV-SENASICA-SAGARPA (currently SADER)] via the Consejo Nacional Consultivo Fitosanitario (CONACOFI) through projects 41011–2017, 41012-2018, 41013-2019, 80124-2020, and 80147-2021 awarded to MA. Additional funds were provided by the Universidad de Valencia, Valencia, Spain via a Distinguished Professor Fellowship to MA (UV-INV-EPC17-548793) and the Consejo Nacional de Ciencia y Tecnología (CONACyT)—Gobierno del Estado de Veracruz FOMIX grant (Project VER-2017-01-292397) to MA. The project was also supported by the Generalitat Valenciana, Valencia, Spain (Project Prometeo/2018/A/133 to AM). Finally, the logistical and financial support of the Instituto de Ecología, A.C. (INECOL) is also acknowledged.Peer reviewe

La reivindicación de las bacterias

Este artículo ha sido posible gracias a una beca otorgada a M. Aluja por la Universidad de Valencia (apoyos, rectoría, estancias temporales de investigadores invitados, subprograma “Atracción de Talento” de VLC-CAMPUS), así como fondos proporcionados por el Consejo Nacional Consultivo Fitosanitario (Proyectos Conacofi-SENASICA 2017/2018) y el Instituto de Ecología, A. C. – Inecol. También de proyectos a A. M. del Ministerio de Ciencia y Competitividad de España (BFU2015-64322-C2-1-R, SAF2015-65878-R), del Instituto de Salud Carlos III de España (PIE14/00045 y AC15/00022), de la Generalitat Valenciana (PrometeoII/20147065) y de Fondos FEDER de la Unión Europea

Influence of Sunlight Incidence and Fruit Chemical Features on Oviposition Site Selection in Mango by Anastrepha obliqua: Implications for Management

With the aim of identifying key factors that determine oviposition decisions by Anastrepha obliqua for management purposes, we conducted a behavioral study under natural/semi-natural field conditions to identify where exactly in the fruit (upper, middle, or lower sections) females preferred to lay eggs in a highly susceptible mango cultivar (“Criollo”), and whether sunlight incidence and fruit chemical compounds influenced oviposition site selection by this pestiferous fly. Females oviposited in shaded, upper fruit sections where pulp had higher total carbohydrate concentrations but similar total protein, lipid, and polyphenol concentrations than non-oviposited sections. Peel had higher overall nutrient and mangiferin/quercetin-3-D-galactoside (polyphenols) concentrations. An untargeted metabolomic analysis of oviposited and non-oviposited fruit sections identified abscisic acid (ABA) and dihydrophaseic acid glucoside, a by-product of ABA catabolism, as potential chemical markers that could play a role in fruit acceptance behaviors by female flies. We conclude that females preferentially oviposit in fruit sections with optimal chemical and environmental conditions for larval development: more carbohydrates and antioxidants such as mangiferin and ferulic acid and lesser sunlight exposure to avoid lethal egg/larval desiccation/overheating. We make specific recommendations for A. obliqua management based on female host selection behavior, a tree pruning scheme exposing fruit to direct sunlight, application of a host marking pheromone, and the use of egg sinks in the orchard

Metagenomic survey of the highly polyphagous Anastrepha ludens developing in ancestral and exotic hosts reveals the lack of a stable microbiota in larvae and the strong influence of metamorphosis on adult gut microbiota

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.This study was principally financed with resources from the Mexican Ministry of Agriculture (SADER), Dirección del Programa Nacional de Moscas de la Fruta (DGSV – SENASICA) via the National Consultative Phytosanitary Council (CONACOFI) through projects 41011–2017, 41012–2018, 41013–2019, 80124–2020, and 80147–2021 awarded to MA. Additional funds were provided by the Asociación de Productores y Empacadores Exportadores de Aguacate de México (APEAM), Project 41010 to MA, the Universidad de Valencia via a Distinguished Professor Fellowship to MA (UV-INV-EPC17-548793), the Consejo Nacional de Ciencia y Tecnología (CONACyT)–Gobierno del Estado de Veracruz FOMIX grant (Project VER-2017-01-292397) to MA, and by the Instituto de Ecología, AC–INECOL. This project was also financed by Generalitat Valenciana (Valencia, Spain), Prometeo/2018/A/133 grant to AM.Peer reviewe

A First Glimpse of the Mexican Fruit Fly Anastrepha ludens (Diptera: Tephritidae) Antenna Morphology and Proteome in Response to a Proteinaceous Attractant

Anastrepha ludens is a key pest of mangoes and citrus from Texas to Costa Rica but the mechanisms of odorant perception in this species are poorly understood. Detection of volatiles in insects occurs mainly in the antenna, where molecules penetrate sensillum pores and link to soluble proteins in the hemolymph until reaching specific odor receptors that trigger signal transduction and lead to behavioral responses. Scrutinizing the molecular foundation of odorant perception in A. ludens is necessary to improve biorational management strategies against this pest. After exposing adults of three maturity stages to a proteinaceous attractant, we studied antennal morphology and comparative proteomic profiles using nano-LC-MS/MS with tandem mass tags combined with synchronous precursor selection (SPS)-MS3. Antennas from newly emerged flies exhibited dense agglomerations of olfactory sensory neurons. We discovered 4618 unique proteins in the antennas of A. ludens and identified some associated with odor signaling, including odorant-binding and calcium signaling related proteins, the odorant receptor co-receptor (Orco), and putative odorant-degrading enzymes. Antennas of sexually immature flies exhibited the most upregulation of odor perception proteins compared to mature flies exposed to the attractant. This is the first report where critical molecular players are linked to the odor perception mechanism of A. ludens

Assessment of the Molecular Responses of an Ancient Angiosperm against Atypical Insect Oviposition: The Case of Hass Avocados and the Tephritid Fly <i>Anastrepha ludens</i>

Anastrepha spp. (Diptera: Tephritidae) infestations cause significant economic losses in commercial fruit production worldwide. However, some plants quickly counteract the insertion of eggs by females by generating neoplasia and hindering eclosion, as is the case for Persea americana Mill., cv. Hass (Hass avocados). We followed a combined transcriptomics/metabolomics approach to identify the molecular mechanisms triggered by Hass avocados to detect and react to the oviposition of the pestiferous Anastrepha ludens (Loew). We evaluated two conditions: fruit damaged using a sterile pin (pin) and fruit oviposited by A. ludens females (ovi). We evaluated both of the conditions in a time course experiment covering five sampling points: without treatment (day 0), 20 min after the treatment (day 1), and days 3, 6, and 9 after the treatment. We identified 288 differentially expressed genes related to the treatments. Oviposition (and possibly bacteria on the eggs’ surface) induces a plant hypersensitive response (HR), triggering a chitin receptor, producing an oxidative burst, and synthesizing phytoalexins. We also observed a process of cell wall modification and polyphenols biosynthesis, which could lead to polymerization in the neoplastic tissue surrounding the eggs