Recently, there has been growing awareness that many animals and plants harbour bacterial symbionts that help protect them against natural enemies. The mushroom-breeding fly Drosophila neotestacea is commonly infected with a virulent parasitic nematode, Howardula aoronymphium. Infections are severe, reducing adult survival and mating success, and until recently virtually all females were rendered sterile. We have discovered that D. neotestacea harbours a strain of the bacterial symbiont Spiroplasma that restores fertility to nematode-parasitized female flies. Spiroplasma appears to be both increasing in frequency and spreading westward across N. America. My thesis examines associations between flies, nematodes and Spiroplasma in British Columbia, which appears to lie at the edge of the range of advancing Spiroplasma infections. I identified Spiroplasma-infected flies in British Columbia for the first time. Sequencing a number of Spiroplasma genes, as well as fly mitochondrial DNA, strongly suggests that the defensive symbiont is spreading westward. Furthermore, high nematode infection rates in BC, as well as laboratory experiments demonstrating the ability of Spiroplasma to restore fertility to nematode-parasitized BC flies, suggest that there is a strong selective pressure for Spiroplasma to continue to spread in BC. I also examined the generality of Spiroplasma-mediated defense by exposing flies to a gram-negative bacterial pathogen, Pectobacterium carotovorum. Exposure dramatically reduced survival regardless of Spiroplasma infection, suggesting that Spiroplasma does not defend against gram-negative bacteria. / Graduate / 0718

Some intracellular symbionts of insects confer host protection from a variety of bacterial, fungal and viral pathogens as well as from predators and parasitoids. Within the cryptic species complex of whiteflies known collectively as Bemisia tabaci is a cosmopolitan invasive agricultural pest, which is commonly infected with the symbiont Rickettsia sp. nr. bellii. Rickettsia swept rapidly through southwestern USA whitefly populations of the MEAM1 species and has been associated in a genotype-dependent manner with increased whitefly fitness and female biased sex ratios. Here we sought to determine whether Rickettsia in MEAM1 might have a defensive role against the general entomopathogenic fungus, Beauvaria bassiana. Nymphs from two lines of whitefly, each with Rickettsia positive (R+) and negative (R-) sublines were exposed to different doses of B. bassiana. The results provided evidence of protection by Rickettsia in one genetic line (MAC1) but not in the other (MAC2). In a third experiment, females of the four sublines were each outcrossed for two generations with males from an outbred whitefly culture, derived from the field within the year, and F2 nymphs from these four new sublines were exposed to the fungus. In this experiment, Rickettsia was protective in both MAC1-O and MAC2-O lines. Taken together, our results suggest the symbiont Rickettsia can confer protection against a generalist entomopathogenic fungus, B. bassiana, and that this protection is conditional on host genotype. To our knowledge, this is the first record of an insect symbiont conferring protection against a generalized and commercially available biological control agent. Bemisia tabaci MEAM1 is a global pest of warm temperate and tropical agriculture, and the prevalence of Rickettsia in many populations of this species could limit the predictability or efficacy of fungal pathogens as a potential management tool.

Endosymbiosis is a pervasive phenomenon that has been a powerful force in insect evolution. In many well studied insect-bacterial associations, the bacteria can serve as reproductive manipulators, nutritional mutualists or defenders of their hosts. Fungi are also frequently associated with insects, and initial estimates suggest that these fungi are hyperdiverse. Saving a handful of examples, however, the functions of these fungi within insect hosts are largely unknown. This dissertation begins with a review that lays the conceptual groundwork for understanding bacterial and fungal endosymbiosis in insects. I make predictions about why one versus the other microbe might serve the insect, given any unique physiological, ecological or evolutionary conditions. I then aim to derive insights about microbial symbiosis by focusing on a particular system, that of brownbanded cockroaches, Supella longipalpa (Blattaria: Blattellidae) and their specialist wasp parasitoids, Comperia merceti (Hymenoptera: Encyrtidae). Here, I identify the symbiotic community of these two insects by using both culture-dependent and independent methods to characterize the vertically transmitted bacterial and fungal associates. Finally, I show that a heritable fungus in C. merceti, long presumed to be a mutualist, is parasitic under laboratory conditions: infected wasps incur fitness costs for housing the fungal symbiont relative to uninfected wasps. Additionally, although the fungus is not horizontally transmitted sexually, it is readily horizontally transmitted from the offspring of infected females to those of uninfected females that are using the same host.

Bt-maize is engineered to express insecticidal toxins derived from the bacterium Bacillus thuringiensis and has been shown to be very effective against pests like Busseola fusca. However, resistance of this pest against Bt-maize has developed and spread throughout South Africa. This study was inspired by the lack of knowledge over the microorganisms associated with the gut of these insects as they play a vital role in insect growth and development. Microbial-derived enzymes may have a role during an insect‟s adaption in different environmental conditions and to new diets. Previous studies suggest (1) that gut bacteria are required for B. thuringiensis-induced mortality in most Lepidoptera species and (2) that the toxicity of B. thuringiensis depends on microbial community interactions within the gut. The aim of this study was to determine the microbial diversity present in the midgut of B. fusca larvae occurring in maize. Busseola fusca larvae were collected from 30 sites throughout South Africa and dissected to collect their midgut contents. Serial dilutions were made of the contents and spread plated onto nutrient agar after which morphotypes were identified. One-hundred and five morphotypes were identified; DNA were extracted from the selected morphotypes and subjected to PCR analysis followed by secquencing. Sequencing results revealed the dominance of Enterococcus spp., specifically Enterococcus casseliflavus and Enterococcus gallinarum, Klebsiella spp., espesially Klebsiella pneumoniae and Klebsiella oxytoca and Bacillus spp. such as .B. thuringiensis and B. subtilis. Other organisms isolated, included Achromobacter spp., Brevudimonas spp., Caulobacter spp., Enterobacter spp., Halomonas spp., Ochrobactrum spp., Pantoea spp., Pseudomonas spp., Serratia spp., Stenotrophomonas spp., Arthrobacter spp., Brevibacterium spp., Leucobacter spp., Microbacterium spp., Planomicrobium spp. and Staphylococcus spp. The microbial diversity of larvae collected at the respective sampling sites were determined with the Shannon diversity index. The data were compared to several factors regarding the sampling sites. No significant differences were observed between the microbial diversities isolated at the respective sites. This may imply that the microbial community within B. fusca larvae are relative consistent throughout the maize production area. It is important to understand the distribution and structure of gut microbial communities within insects and whether the gut community is influenced by the geographical distribution of the insects. A better understanding of the distribution of the insects and community structure of their gut microbiota may aid in the development of better insect control strategies. / MSc (Environmental Sciences), North-West University, Potchefstroom Campus, 2015

Bt-maize is engineered to express insecticidal toxins derived from the bacterium Bacillus thuringiensis and has been shown to be very effective against pests like Busseola fusca. However, resistance of this pest against Bt-maize has developed and spread throughout South Africa. This study was inspired by the lack of knowledge over the microorganisms associated with the gut of these insects as they play a vital role in insect growth and development. Microbial-derived enzymes may have a role during an insect‟s adaption in different environmental conditions and to new diets. Previous studies suggest (1) that gut bacteria are required for B. thuringiensis-induced mortality in most Lepidoptera species and (2) that the toxicity of B. thuringiensis depends on microbial community interactions within the gut. The aim of this study was to determine the microbial diversity present in the midgut of B. fusca larvae occurring in maize. Busseola fusca larvae were collected from 30 sites throughout South Africa and dissected to collect their midgut contents. Serial dilutions were made of the contents and spread plated onto nutrient agar after which morphotypes were identified. One-hundred and five morphotypes were identified; DNA were extracted from the selected morphotypes and subjected to PCR analysis followed by secquencing. Sequencing results revealed the dominance of Enterococcus spp., specifically Enterococcus casseliflavus and Enterococcus gallinarum, Klebsiella spp., espesially Klebsiella pneumoniae and Klebsiella oxytoca and Bacillus spp. such as .B. thuringiensis and B. subtilis. Other organisms isolated, included Achromobacter spp., Brevudimonas spp., Caulobacter spp., Enterobacter spp., Halomonas spp., Ochrobactrum spp., Pantoea spp., Pseudomonas spp., Serratia spp., Stenotrophomonas spp., Arthrobacter spp., Brevibacterium spp., Leucobacter spp., Microbacterium spp., Planomicrobium spp. and Staphylococcus spp. The microbial diversity of larvae collected at the respective sampling sites were determined with the Shannon diversity index. The data were compared to several factors regarding the sampling sites. No significant differences were observed between the microbial diversities isolated at the respective sites. This may imply that the microbial community within B. fusca larvae are relative consistent throughout the maize production area. It is important to understand the distribution and structure of gut microbial communities within insects and whether the gut community is influenced by the geographical distribution of the insects. A better understanding of the distribution of the insects and community structure of their gut microbiota may aid in the development of better insect control strategies. / MSc (Environmental Sciences), North-West University, Potchefstroom Campus, 2015

The Bemisia tabaci (Gennadius) sibling species group is known to comprise several morphologically undistinguishable mitotypes which can be separated into seven major phylogeographic clades using the 3' half of the mitochondrial cytochrome oxidase I gene. B. tabaci is the only vector of begomoviruses; it transmits the complex of viruses that cause the cotton leaf curl disease, which has rapidly spread from Pakistan to the Philippines, at southeast of Asia, in the last decade. The study of B. tabaci mitotypes has been limited to variants of worldwide distribution and those associated to agroecosystems, however, the study of indigenous mitotypes has been scarce. This dissertation provides a comprehensive study of the phylogeography and population biology of mitotypes belonging to two major phylogeographic clades, the Asia II and the Americas. The Asia II major clade contains the highest number of mitotypes, in contrast, there is a large gap in knowledge about mitotypes associated to highly endemistic niches in the Americas. To study the population biology of mitotypes belonging to the Asia II major phylogeographic clade, two fragments of the mtCOI gene were amplified by polymerase chain reaction (PCR) for adult whiteflies sampled from mono and multi-cropping systems in the provinces of Punjab and Sindh in Pakistan. Phylogenetic analyses suggested that three indigenous mitotypes were distinctively distributed across ecosystems of Pakistan. The Asia II-5 and II-7 were found restricted to multi-cropping systems of Lahore, while the Asia II-1 was found widespread throughout the cotton growing region of Pakistan. Moreover, population analyses suggested the Asia II-1 is undergoing demographic expansion following a recent selective sweep or bottleneck. This event explains the predominance of Asia II-1 in Pakistan and its spread towards the southern province of Sindh. Additionally, differences in DNA polymorphism and diversity between mtCOI fragments derived in dissimilar evolutionary pairwise distances, suggestive of future implications in the “species” delimitation at a global scale when choosing one fragment over the other. The endosymbiotic bacteria assemblages associated to indigenous mitotypes Asia II-1, II-5 and II-7 were studied by analysis of 16S rRNA profiles. Besides the primary symbiont Portiera, Arsenophonus was detected almost fixed in the studied populations and several unique strains of Arsenophonus were detected in Asia II-5 and II-7, suggesting possible unique environmental adaptation capacities of these mitotypes. Hierarchical clustering of 16S rRNA profiles, proposed host-based and environmental-related differentiation. Additionally, the disruption of parallel cladogenesis between the primary symbiont and B. tabaci, disallows rejection of the hypothesis that gene flow among B. tabaci mitotypes occurs. To study the population biology of indigenous mitotypes belonging to the Americas major clade, adult whiteflies were sampled from ecosystems of nine provinces in Ecuador. Based on phylogenetic analyses, three indigenous and one invasive mitotype were detected. Among the indigenous, a previously unrecognized mitotype, named ECU3, was found. Moreover, mitotypes were found coexisting in five locations, and the invasive B is thought to have displaced endemic mitotypes to the northern and eastern coastal habitats of Ecuador.

The house dust mites (HDM; Dermatophagoides farinae and Dermatophagoides pteronyssinus) obtain nutrients from the debris of the skin, hairs and nails, that get off the human and animal body. These debris are covered by microorganisms and the microorganisms are the key factor in the survival of HDM in human-made environments. In this study we made manipulative experiments with the extract from spent growth medium (SPGM). SPGM is the medium after mite cultivation, composed from mite feces, debris of the diet, dead mite bodies and microorganisms. The extract from SPGM (one and three-month-old mite cultures) was used as the source of microorganism to transfer them into diet of D. farinae a D. pteronyssinus. The composition of the bacterial and fungal microbiomes differed between the HDM species, but the SPGM extract addition into diet influenced only the bacterial profile of D. farinae. In the D. farinae microbiome of specimens on SPGM-treated diets compared to those of the control situation, the Lactobacillus spp. profile decreased, while the Cardinium, Staphylococcus, Acinetobacter, and Sphingomonas profiles increased. The addition of SPGM extract decreased the microbial respiration in the microcosms with and without mites in almost all cases. Adding SPGM did not influence the population growth of D. farinae,...

De nombreuses bactéries entrent en symbiose avec les métazoaires colonisant les habitats à base chimiosynthétique dans l'océan profond. Les hôtes auxquels elles apportent le carbone organique deviennent ainsi dépendants des bactéries sulfo-oxydantes et/ou méthanotrophes. Pour assurer la continuité de ces associations et la colonisation de nouveaux sites, des stratégies diverses de dispersion ont été développées par les animaux. Deux types de transmission des bactéries symbiotiques existent : la transmission verticale où elles sont transmises via les gamètes, et la transmission horizontale où elles sont acquises à partir de l¿environnement, depuis des populations de bactéries libres ou relarguées par d'autres hôtes. Cette thèse vise à répondre à des questions concernant les cycles de vie des symbiontes. La diversité et la distribution des formes libres de symbiontes et des bactéries apparentées dans plusieurs habitats réduits ont été étudiées par l¿analyse des séquences de l'ARNr 16S des bactéries colonisant des substrats organiques déployés dans l'Atlantique et la Méditerranée. La transmission maternelle des symbiontes chez le bivalve vésicomyidé Isorropodon bigoti du golfe de Guinée a été confirmée par l'observation et l'identification des symbiontes dans les ovocytes et dans les stades post-larvaires. Enfin, l'effet des stress chimique, thermique et de la remontée sur la dynamique des populations de symbiontes sulfo-oxydants et méthanotrophes chez la moule Bathymodiolus azoricus a été analysé par les techniques de FISH 3D et de pyroséquençage. Cette thèse a permis de mieux comprendre des cycles de vie des bactéries symbiotiques dans et en dehors de leur hôtes animaux. / Metazoans colonizing deep-sea reducing habitats often employ chemosymbiotic bacterial associations. Hosts become dependent upon their sulfur-oxidizing and/or methanotrophic symbionts, which provide organic carbon compounds. Various larval dispersal strategies have evolved in the hosts, ensuring the colonization of new sites. The continuity of the symbiotic association is maintained by symbiont transmission. Symbionts may pass directly to the host’s progeny via gametes (vertical transmission) or may be acquired from the environment as free-living forms or as those released from other hosts (horizontal transmission). This work answers several questions about the lifecycles of symbionts regarding the diversity of symbiont-related bacteria in environmental bacterial communities; the localization and dynamics of symbionts in host tissues depending on their transmission mode; or after abiotic stresses applied to the holobiont.The diversity and the distribution of free-living symbionts and their close relatives from several chemosynthesis-based habitats has been analysed by 454 pyrosequencing of the 16S rRNA of bacteria colonizing plant-derived substrates in the Northern Atlantic and Mediterranean. The trans-ovarial transmission has been detailed in the clam Isorropodon bigoti by the identification of symbionts within oocytes and in the forming gills of their post-larvae. Finally, the influence of several abiotic stresses in Bathymodiolus azoricus mussels on the dynamics of their symbionts has been investigated by FISH and pyrosequencing. This PhD presents new data regarding various aspects of the life cycle of chemosynthetic symbionts inside and outside their metazoan hosts.

Parasitoides interferem no sistema imunológico de seus hospedeiros, influenciando a expressão de genes relacionados à resposta celular e humoral, podendo interferir na relação hospedeiro - microbiota intestinal. Além disso, parasitoides induzem alterações fisiológicas no hospedeiro que alteram o consumo e a utilização de alimento, e que podem influenciar a microbiata intestinal do mesmo. Alterações nessa microbiota poderiam afetar as relações e contribuições ao hospedeiro e, consequentemente, influenciar o desenvolvimento do próprio parasitoide. O objetivo deste trabalho foi o de verificar o efeito do parasitismo por Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) na estrutura e no potencial funcional de contribuição da microbiota intestinal de Diatraea saccharalis (F.) (Lepidoptera: Crambidae), hospedeiro permissivo, e de Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), hospedeiro não-permissivo. Além disso, buscou-se verificar se as secreções utilizadas pelo parasitoide (veneno, fluidos do cálice e virus simbionte) na regulação hospedeira estariam associadas à manipulação da microbiota intestinal do hospedeiro. O efeito do parasitismo na microbiota intestinal associada às porções antero-mediana e posterior do intestino dos hospedeiros estudados foi avaliado na fase inicial (1 DAP - dia após o parasitismo), intermediária (5 DAP) e final (9 DAP) do desenvolvimento larval do parasitoide. A avaliação foi feita por meio da comparação da diversidade e abundância de bactérias associadas ao trato intestinal de D. saccharalis e S. frugiperda parasitadas ou não por C. flavipes. A caracterização das bactérias foi feita via análise metagenômica em plataforma Illumina MiSeq utilizando a região V4 do gene ribossomal 16S. O pacote de softwares QIIME foi utilizado para a atribuição taxonômica das mesmas e o potencial funcional foi inferido por meio do software PICRUSt. O parasitismo afetou a abundância e diversidade de unidades taxonômicas operacionais (UTOs) da microbiota intestinal da porção antero-mediana e posterior de ambos hospedeiros. As alterações observadas para as duas regiões intestinais investigadas não seguiram o mesmo padrão ao longo do desenvolvimento do parasitoide. As análises realizadas também demonstraram que as alterações da microbiota induzidas pelo parasitismo refletiram em alterações significativas no potencial funcional de contribuição da microbiota associada ao trato digestivo de D. saccharalis e S. frugiperda. As análises da microbiota de lagartas pseudo-parasitadas demonstraram que as secreções maternas injetadas pela fêmea do parasitoide no momento do parasitismo estão envolvidas, pelo menos parcialmente, com os processos que levam às modificações na diversidade e abundância da microbita intestinal hospedeira, assim como de seu potencial de contribuição funcional. Esses resultados indicam que outros fatores/alterações produzidos em condições normais de parasitismo, seja pela influência de secreções de teratócitos e das próprias larvas do parasitoide em desenvolvimento também estão envolvidos na manipulação da microbiota hospedeira. Várias das alterações observadas no potencial de contribuição da microbiota intestinal do hospedeiro podem refletir sua qualidade nutricional e, consequentemente, favorecer sua exploração pelo parasitoide. Assim, o processo de regulação hospedeira por parasitoides se estende ao conjunto de organismos associados que compõem o holobionte representado pela lagarta hospedeira. / Parasitoids interfere with the immune system of their hosts by influencing the expression of genes related to cellular and humoral responses, which may interfere with the host - gut microbiota relationship. Furthermore, parasitoids induce physiological changes in the host, modifying food consumption and utilization, influencing then the host gut microbiota. These changes can affect the relationship and contributions of the gut microbiota to the host and therefore influence parasitoid development. This study aimed to evaluate the effect of parasitism by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) in the structure and potential functional contribution of the gut microbiota of the permissive host Diatraea saccharalis (F.) (Lepidoptera: Crambidae) and the non-permissive host Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) . In addition, the participation of the secretions female parasitoids (venon, calyx fluid and symbiotic virus) use in host regulation in the manipulation of the host gut microbiota was also investigated. The effects of host parasitization on the microbiota associated with the anterior (foregut-midgut) and posterior (hindgut) portions of host gut were evaluated at the early (1 DAP - day after parasitism), intermediate (5 DAP) and final (9 DAP) stages of parasitoid larval development. The diversity and abundance of the gut microbiota of D. saccharalis and S. frugiperda was compared in between parasitized and non-parasitized larvae by C. flavipes. The gut microbiota was characterized by sequencing the V4 region of the 16S ribosomal gene using the Illumina MiSeq platform. The software package QIIME was used for taxonomic attribution and the PICRUSt software was used to infer the potential funcional contribution of the gut microbiota. Host parasitization affected the abundance and diversity of operational taxonomic units (OTUs) of the two gut regions investigated (foregut-midgut and hindgut) in both hosts. The changes observed for both gut regions did not follow the same pattern throughout parasitoid development. Changes in the gut microbiota induced by parasitization reflected in significant changes in the potential of the functional contribution of the gut microbiota associated with D. saccharalis and S. frugiperda. Analyses of pseudo-parasitized larvae demonstrated that the maternal secretions female parasitoids inject when ovipositing are involved, at least partially, with the processes that lead to changes in the abundance, diversity and potential functional contribution of the host gut microbita. These results indicate that other factors / changes produced during normal parasitization, such as secretions from teratocytes and/or the developing parasitoid larvae can also be involved in the manipulation of host gut microbiota. Several of the changes observed in the potential contribution of the host gut microbiota may reflect its nutritional quality and therefore favor host exploitation by parasitoids. Thus, the process of host regulation by parasitoids also involves the regulation of the gut-associated bacteria, which altogether comprise the holobionte represented by the host larvae.

Symbiosis is one of the main players in evolution and ecology of organisms. Such intimate interactions may be diverse and have a great impact in biological diversification. One of the main associations that occur in nature is that of insects and microbes. Insect associated microbes are, capable of altering a wide range of physiological, behavioral, ecological and evolutionary events for their hosts. Two very common insect microbial symbionts are Wolbachia and Spiroplasma. Wolbachia is also common to other arthropods and nematodes. To better understand how these relations could influence the behavior of insects, we selected two biological systems to investigate how these symbionts can interfere in the host - parasitoid interactions. We investigated the behavior of two species of parasitoids, Aphelinus asychis (Hymenoptera: Aphididae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) when exploting patches with their respective hosts, Aphis citricidus (Hemiptera: Aphididae) and Anagasta kuehniella (Lepidoptera: Pyralidae). In the first case we looked into how Spiroplasma infecting hosts, and in the second case how Wolbachia infecting the parasitoid may affect parasitoid patch exploitation. We recorded the wasp\'s behaviors when exploiting their patches, as well as the aphid defensive behavior in response to parasitoid attack. Our data demonstrate Spiroplasma and Wolbachia influence the parasitoid patch exploitation decisions. Spiroplasma also affected the defense behavior and aggressiveness of A. citricidus in response to A. asychis attack. Wolbachia increased the patch residence time and reduced the successful parasitization of host eggs in T. pretiosum. The understanding of such effects will certainly contribute to provide a better knowledge of the outcome of the associations of insects with microbial symbionts, providing ground base for the proper exploitation of such interactions for biological control purposes. / A simbiose é um dos principais agentes na evolução e ecologia de organismos. Tais interações são muito íntimas, podendo ser muito diversas e ter grandes impactos na diversidade biológica. Uma das principais associações que ocorrem na natureza é aquela entre insetos e microrganismos. Microrganismos associados a insetos são capazes de alterar uma gama de eventos fisiológicos, comportamentais, ecológicos e evolutivos em seus hospedeiros. Dois simbiontes de insetos muito comuns são Wolbachia e Spiroplasma. Wolbachia é também muito comum a outros artrópodes e nematoides. Para melhor compreender como essas relações podem influenciar o comportamento de insetos, dois sistemas biológicos foram selecionados para investigar como esses simbiontes podem interferir nas interações hospedeiro-parasitoide. O comportamento de duas espécies de parasitoides, Aphelinus asychis (Hymenoptera: Aphididae) e Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) foi investigado quando explorando patches com seus respectivos hospedeiros, Aphis citricidus (Hemiptera: Aphididae) e Anagasta kuehniella (Lepidoptera: Pyralidae). No primeiro caso foi investigado como a infecção do hospedeiro por Spiroplasma, e no segundo caso como a infecção do parasitoide por Wolbachia, afetariam a exploração da patch pelos parasitoides. O comportamento dos parasitoides ao explorarem suas patches foi registrado, assim como os comportamentos de defesa dos pulgões em resposta ao ataque do parasitoide. Os dados obtidos demonstraram que Spiroplasma afetaram o comportamento de defesa e a agressividade de A. citricidus em resposta aos ataques de A. asychis. Wolbachia aumentou o tempo de residência e reduziu o sucesso de parasitismo de ovos do hospedeiro por T. pretiosum. A compreensão de tais efeitos certamente contribuirá para o melhor entendimento dos efeitos da associação de insetos a simbiontes, fornecendo bases sólidas para a melhor exploração de tais interações para propósitos de controle biológico de pragas.