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Facultative bacterial endosymbionts are associated with many arthropods and are primarily transmitted vertically from mother to offspring. However, phylogenetic affiliations suggest that horizontal transmission must also occur. Such horizontal transfer can have important biological and agricultural consequences when endosymbionts increase host fitness. So far horizontal transmission is considered rare and has been difficult to document. Here, we use fluorescence in situ hybridization (FISH) and multi locus sequence typing (MLST) to reveal a potentially common pathway of horizontal transmission of endosymbionts via parasitoids of insects. We illustrate that the mouthparts and ovipositors of an aphelinid parasitoid become contaminated with Wolbachia when this wasp feeds on or probes Wolbachia-infected Bemisia tabaci AsiaII7, and non-lethal probing of uninfected B. tabaci AsiaII7 nymphs by parasitoids carrying Wolbachia resulted in newly and stably infected B. tabaci matrilines. After they were exposed to infected whitefly, the parasitoids were able to transmit Wolbachia efficiently for the following 48 h. Whitefly infected with Wolbachia by parasitoids had increased survival and reduced development times. Overall, our study provides evidence for the horizontal transmission of Wolbachia between insect hosts by parasitic wasps, and the enhanced survival and reproductive abilities of insect hosts may adversely affect biological control programs.

Recent studies on yeast-insect associations demonstrated that social wasps of the genera Polistes and Vespula act as a reservoir for the conservation of yeasts and as vectors capable of transferring such yeasts on the grapes. This work aimed to assess yeast species associated with social wasps and to obtain new strains to be used as bio-protection agents in winemaking. The wine yeast communities present on the exoskeleton, intestine of social wasps, and on the surface of grapes sampled in the vineyards of three Tuscan wineries were determined. Regardless of the wasp species, yeasts were mostly associated with female workers and found mainly in their intestine (up to 7 × 10 5  CFU/mL). The identification revealed 20 species belonging to 10 genera; Aureobasidium pullulans and Metschnikowia pulcherrima were isolated from wasps of all the wineries, the latter occurring at the highest frequency. Strain-level characterization highlighted that three strains present on grapes were also present in the gut of wasps from the same vineyard. All the isolated M. pulcherrima strains underwent in vitro tests to select the most suitable for use as bio-protective cultures. Three strains showed good inhibitory activity against Kloeckera apiculata and Brettanomyces bruxellensis ; hence, they were selected for bio-protection trials on artificially contaminated grapes. Results highlighted the reduction of non- Saccharomyces populations, suggesting the effectiveness of M. pulcherrima as a biocontrol agent. The study confirmed the role of social wasps as yeast vectors in the vineyard and as a reservoir of yeast strains to be exploited for biotechnological applications in oenology. Key points • Social wasps can carry yeast strains that are also present on the surface of grapes •  Metschnikowia pulcherrima was found within the wasp gut as the prevalent yeast species •  M. pulcherrima proved to be a suitable biocontrol agent on grapes

Koinobiont endoparasitoids regulate the physiology of their hosts through altering host immuno-metabolic responses, processes which function in tandem to shape the composition of the microbiota of these hosts. Here, we employed 16S rRNA and ITS amplicon sequencing to investigate whether parasitization by the parasitoid wasps, Diachasmimorpha longicaudata (Ashmaed) (Hymenoptera: Braconidae) and Psyttalia cosyrae (Wilkinson) (Hymenoptera: Braconidae), induces gut dysbiosis and differentially alter the gut microbial (bacteria and fungi) communities of an important horticultural pest, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). We further investigated the composition of bacterial communities of adult D. longicaudata and P. cosyrae to ascertain whether the adult parasitoids and parasitized host larvae share microbial taxa through transmission. We demonstrated that parasitism by D. longicaudata induced significant gut perturbations, resulting in the colonization and increased relative abundance of pathogenic gut bacteria. Some pathogenic bacteria like Stenotrophomonas and Morganella were detected in both the guts of D. longicaudata-parasitized B. dorsalis larvae and adult D. longicaudata wasps, suggesting a horizontal transfer of microbes from the parasitoid to the host. The bacterial community of P. cosyrae adult wasps was dominated by Arsenophonus nasoniae, whereas that of D. longicaudata adults was dominated by Paucibater spp. and Pseudomonas spp. Parasitization by either parasitoid wasp was associated with an overall reduction in fungal diversity and evenness. These findings indicate that unlike P. cosyrae which is avirulent to B. dorsalis, parasitization by D. longicaudata induces shifts in the gut bacteriome of B. dorsalis larvae to a pathobiont-dominated community. This mechanism possibly enhances its virulence against the pest, further supporting its candidacy as an effective biocontrol agent of this frugivorous tephritid fruit fly pest.

There is increasing evidence that host–parasitoid interactions can have a pronounced impact on the microbiome of host insects, but it is unclear to what extent this is caused by the host and/or parasitoid. Here, we compared the internal and external microbiome of caterpillars of Pieris brassicae and Pieris rapae parasitized by Cotesia glomerata or Cotesia rubecula with nonparasitized caterpillars. Additionally, we investigated the internal and external microbiome of the parasitoid larvae. Both internal and external bacterial densities were significantly higher for P. brassicae than P. rapae, while no differences were found between parasitized and nonparasitized caterpillars. In contrast, parasitism significantly affected the composition of the internal and external microbiome of the caterpillars and the parasitoid larvae, but the effects were dependent on the host and parasitoid species. Irrespective of host species, a Wolbachia species was exclusively found inside caterpillars parasitized by C. glomerata, as well as in the corresponding developing parasitoid larvae. Similarly, a Nosema species was abundantly present inside parasitized caterpillars and the parasitoid larvae, but this was independent of the host and the parasitoid species. We conclude that parasitism has pronounced effects on host microbiomes, but the effects depend on both the host and parasitoid species.

The reproductive ecology of Saccharomyces cerevisiae is still largely unknown. Recent evidence of interspecific hybridization, high levels of strain heterozygosity, and prion transmission suggest that outbreeding occurs frequently in yeasts. Nevertheless, the place where yeasts mate and recombine in the wild has not been identified. We found that the intestine of social wasps hosts highly outbred S. cerevisiae strains as well as a rare S. cerevisiae×S. paradoxus hybrid. We show that the intestine of Polistes dominula social wasps favors the mating of S. cerevisiae strains among themselves and with S. paradoxus cells by providing a succession of environmental conditions prompting cell sporulation and spores germination. In addition, we prove that heterospecific mating is the only option for European S. paradoxus strains to survive in the gut. Taken together, these findings unveil the best hidden secret of yeast ecology, introducing the insect gut as an environmental alcove in which crosses occur, maintaining and generating the diversity of the ascomycetes.

The blue-gum chalcid Leptocybe invasa Fisher & LaSalle (Hymenoptera: Eulophidae) is a gall wasp pest of Eucalyptus species, likely native to Australia. Over the past 15 years it has invaded 39 countries on all continents where eucalypts are grown. The worldwide invasion of the blue gum chalcid was attributed to a single thelytokous morphospecies formally described in 2004. Subsequently, however, males have been recorded in several countries and the sex ratio of field populations has been found to be highly variable in different areas. In order to find an explanation for such sex ratio differences, populations of L. invasa from a broad geographical area were screened for the symbionts currently known as reproductive manipulators, and both wasps and symbionts were genetically characterized using multiple genes. Molecular analyses suggested that L. invasa is in fact a complex of two cryptic species involved in the rapid and efficient spread of the wasp, the first recovered from the Mediterranean region and South America, the latter from China. All screened specimens were infected by endosymbiotic bacteria belonging to the genus Rickettsia. Two closely related Rickettsia strains were found, each infecting one of the two putative cryptic species of L. invasa and associated with different average sex ratios. Rickettsia were found to be localized in the female reproductive tissues and transovarially transmitted, suggesting a possible role of Rickettsia as the causal agent of thelytokous parthenogenesis in L. invasa. Implications for the variation of sex ratio and for the management of L. invasa are discussed.

The study of microbiota of social insects under different ecological conditions can provide important insights into the role of microbes in their biology and behavior. Polistes is one of the most widely distributed and extensively studied genera of social wasps, yet a comprehensive study on the microbiota of any species of Polistes or any primitively eusocial wasp is missing. Polistes wattii is an Asian wasp, which hibernates in winter and exhibits a biannual nest founding strategy. It is often parasitized by the strepsipteran endoparasite/parasitoid Xenos gadagkari , which changes the morpho-physiology and behavior of their hosts . In this study, we employ 16S rRNA amplicon sequencing, using the Oxford Nanopore platform, to study the microbial community of P. wattii and investigate the effects of seasonality, sex, and Xenos parasitism. We show that the microbiota differs in females from solitary foundress spring nests and multiple foundress summer nests. The microbiota also differs in males and females. Finally, we show that X. gadagkari parasitism replaces and homogenizes the microbiota of P. wattii. Unlike the unparasitized wasps, the microbiota of X. gadagkari parasitoids and parasitized wasps are dominated by Wolbachia and Providencia. Although the normal microbiota of P. wattii resembles that of highly eusocial vespid wasps, we show that the microbiota of parasitized P. wattii becomes more like the microbiota of strepsipterans. Therefore, it appears that X. gadagkari and other such strepsipteran parasitoids may have a bigger impact on the biology of their hosts than previously thought.

Wolbachia is an endosymbiotic bacterium found in many species of arthropods and manipulates its host reproduction. Cytoplasmic incompatibility (CI) is one of the most common manipulations that is induced when an uninfected female mates with a Wolbachia-infected male. The CI factors (cifA and cifB genes) are encoded by phage WO that naturally infects Wolbachia. Here, we questioned whether an environmental factor (temperature) or host factor (male age) affected the strength of the CI phenotype in the ectoparasitoid wasp, Habrobracon hebetor. We found that temperature, but not male age, results in reduced CI penetrance. Consistent with these results, we also found that the expression of the cif CI factors decreased in temperature-exposed males but was consistent across aging male wasps. Similar to studies of other insect systems, cifA showed a higher expression level than cifB, and male hosts showed increased cif expression relative to females. Our results suggest that prophage WO is present in the Wolbachia-infected wasps and expression of cif genes contributes to the induction of CI in this insect. It seems that male aging has no effect on the intensity of CI; however, temperature affects Wolbachia and prophage WO titers as well as expression levels of cif genes, which modulate the CI level.

Honey-feeding social insects such as honey bees and bumble bees have conserved gut bacterial communities that are transmitted among nestmates. These bacteria benefit hosts by providing defense against pathogens and potentially by contributing to pollen digestion. The bacterial communities of wasps are less studied. Whereas most wasps are carnivorous and consume nectar, honey wasps ( Brachygastra spp.) store and eat honey. Here, we address the consequences of this dietary shift for the gut community. Using field collections of Mexican honey wasps and other co-occurring wasps, we found that honey wasps have distinctive gut bacterial communities. These include several bacteria most closely related to bacteria in bumble bees, suggesting their acquisition via host-switching. Solitary wasps and social wasps that do not make honey have smaller gut communities dominated by environmental bacteria, suggesting that honey feeding has shaped the gut bacterial communities of honey wasps.

The endoparasitoid Asecodes hispinarum (Bouček) (Hymenoptera: Eulophidae) serves as an effective biological control agent against Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae), a notorious palm pest. Endosymbionts found in parasitoids and their hosts have attracted significant attention due to their substantial influence on biocontrol efficacy. In this study, we employed 16S rRNA sequencing, polymerase chain reaction, and fluorescence in situ hybridization to assess the symbiotic bacteria composition, diversity, phylogeny, and localization in A. hispinarum and its host B. longissima. Our findings showed significant differences in the richness, diversity, and composition of symbiotic bacteria among different life stages of B. longissima. Notably, the bacterial richness, diversity, and composition of A. hispinarum was similar to that of B. longissima. Firmicutes and Proteobacteria were the dominant phyla, while Wolbachia was the dominant genera across the parasitoid and host. It was discovered for the first time that Wolbachia was present in A. hispinarum with a high infection rate at ≥ 96.67%. Notably, the Wolbachia strain in A. hispinarum was placed in supergroup A, whereas it was categorized under supergroup B in B. longissima. Furthermore, Wolbachia is concentrated in the abdomen of A. hispinarum, with particularly high levels observed in the ovipositors of female adults. These findings highlight the composition and diversity of symbiotic bacteria in both A. hispinarum and its host B. longissima, providing a foundation for the development of population regulation strategies targeting B. longissima. Graphical Abstract