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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.

Among tephritid fruit flies, hybridization has been found to produce local adaptation and speciation, and in the case of pest species, induce behavioral and ecological alterations that can adversely impact efficient pest management. The fraterculus species group within Anastrepha (Diptera: Tephritidae), is a rapidly radiating aggregate, which includes cryptic species complexes, numerous sister species, and several pest species. Molecular studies have highlighted the possibility of introgression between A. fraterculus and A. obliqua. Reproductive isolation has been studied among morphotypes of the A. fraterculus species complex as a tool for species delimitation. Here we examined the existence and strength of prezygotic and postzygotic isolation between sympatric populations of two closely related species within the highly derived fraterculus group (A. fraterculus and A. obliqua), coexisting in nature. Although adults of both species showed a strong tendency for assortative mating, a small proportion of hybrid pairings in both directions were observed. We also observed asymmetric postzygotic isolation, with one hybrid cross displaying a strong reduction in fecundity and F1 egg fertility. Survival was greater for the progeny of homotypic and hybrid crosses in the maternal host. There was a marked female biased sex ratio distortion for both F1 hybrid adults. Hybridization between A. fraterculus and A. obliqua in nature may be difficult but possible; these two species display stronger reproductive isolation than all pairs of species previously examined in the A. fraterculus species complex. Asymmetric postzygotic isolation is suggestive of Wolbachia mediated cytoplasmic incompatibilities that may be exploited in area-wide pest management.

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