The oriental fruit fly, Bactrocera dorsalis (Hendel), and marula fruit fly, Ceratitis cosyra (Walker), are major fruit-infesting tephritids across sub-Saharan Africa. Biological control of these pests using parasitic wasps has been widely adopted but with varying levels of success. Most studies investigating host-parasitoid models have focused on functional and evolutionary aspects leaving a knowledge gap about the physiological mechanisms underpinning the efficacy of parasitoids as biocontrol agents of tephritids. To better understand these physiological mechanisms, we investigated changes in the cellular immune responses of C. cosyra and B. dorsalis when exposed to the parasitic wasps, Diachasmimorpha longicaudata (Ashmaed) and Psyttalia cosyrae (Wilkinson). We found that B. dorsalis was more resistant to parasitisation, had a higher hemocyte count, and encapsulated more parasitoid eggs compared to C. cosyra, achieving up to 100% encapsulation when exposed to P. cosyrae. Exposing B. dorsalis to either parasitoid species induced the formation of a rare cell type, the giant multinucleated hemocyte, which was not observed in C. cosyra. Furthermore, compared to P. cosyrae-parasitized larvae, those of both host species parasitized by D. longicaudata had lower encapsulation rates, hemocyte counts and spreading abilities and yielded a higher number of parasitoid progeny with the highest parasitoid emergence (72.13%) recorded in C. cosyra. These results demonstrate that cellular immune responses are central to host-parasitoid interaction in tephritid fruit flies and further suggest that D. longicaudata presents greater potential as a biocontrol agent of B. dorsalis and C. cosyra in horticultural cropping systems.

Parasitoids are promising biocontrol agents of the devastating fruit fly, Bactrocera dorsalis. However, parasitoid performance is a function of several factors, including host-associated symbiotic bacteria. Providencia alcalifaciens, Citrobacter freundii, and Lactococcus lactis are among the symbiotic bacteria commonly associated with B. dorsalis, and they influence the eco-physiological functioning of this pest. However, whether these bacteria influence the interaction between this pest and its parasitoids is unknown. This study sought to elucidate the nature of the interaction of the parasitoids, Fopius arisanus, Diachasmimorpha longicaudata, and Psyttlia cosyrae with B. dorsalis as mediated by symbiotic bacteria. Three types of fly lines were used: axenic, symbiotic, and bacteria-mono-associated (Lactococcus lactis, Providencia alcalifaciens, and Citrobacter freundii). The suitable stages of each fly line were exposed to the respective parasitoid species and reared until the emergence of adult flies/parasitoids. Thereafter, data on the emergence and parasitoid fitness traits were recorded. No wasps emerged from the fly lines exposed to P. cosyrae. The highest emergence of F. arisanus and D. longicaudata was recorded in the L. lactis fly lines. The parasitoid progeny from the L. lactis and P. alcalifaciens fly lines had the longest developmental time and the largest body size. Conversely, parasitoid fecundity was significantly lower in the L. lactis lines, whereas the P. alcalifaciens lines significantly improved fecundity. These results elucidate some effects of bacterial symbionts on host–parasitoid interactions and their potential in enhancing parasitoid-oriented management strategies against B. dorsalis.

Background Koinobiont endoparasitoids regulate the physiological functioning of their hosts through altering metabolism and immune responses, processes which function in tandem to shape the structure and composition of the microbial communities of these hosts. Here we investigated the hypothesis that parasitisation by the virulent Diachasmimorpha longicaudata and the avirulent Pystallia cosyrae induce gut dysbiosis and differentially alter the gut microbial communities of an important horticultural pest, the oriental fruit fly, Bactrocera dorsalis. Consequently, we employed 16S rRNA and ITS amplicon sequencing to investigate the effect of parasitisation on the bacterial and fungal communities of B. dorsalis, respectively. We further investigated the bacterial communities of D. longicaudata and P. cosyrae using 16S rRNA sequencing. Results Exposure to both parasitoids induced perturbations in the microbial communities of B. dorsalis. The gut bacteriome of B. dorsalis larvae shifted from an Anoxybacillus, Acetobacter and Acinetobacter dominated community to one dominated by the generaMorganella, Stenotrophomonas, Weissella and Pantoea. These effects were especially more pronounced in the D. longicaudata-parasitised larvae compared to those parasitized by P. cosyrae. The diversity and abundance of the fungal community was negatively influenced by parasitisation with an overall reduction in fungi diversity, richness, and evenness. We found an increase in the abundance of Sacchromyces species in larvae parasitized by both wasps compared to the unparasitised controls. On the other hand, the bacterial communities of both parasitoids were less diverse. Arsenophonus nasoniaewas the dominant bacterium in P. cosyrae whereas Paucibacter and Pseudomonas species dominated the bacteriome of D. longicaudata. Conclusion This study presents the first report of the microbial communities of D. longicaudata and P. cosyrae as well as parasitism-induced gut perturbations in B. dorsalis, revealing host gut homeostasis as a possible driver of parasitoid virulence in this invasive pest.