Coral reefs are among the most diverse marine ecosystems, but they are threatened by climate change. The foundation of reef ecosystems is the coral holobiont or metaorganism that consists of the coral animal host, photosynthetic microalgae, bacteria, and viruses (among other organisms). While microalgae provide the energy for corals to build the massive three-dimensional skeletons, bacteria support functions related to metabolism, immunity, and environmental adaptation. Conversely, the function of viruses is less well understood. Although viruses were previously associated with coral disease and bleaching, we are missing an overall understanding of the diversity and identity of viruses associated with corals, in particular for understudied areas such as the Red Sea. Here we characterized coral-associated viral community composition using a large metagenomic and metatransciptomic dataset covering > 1 billion sequences across > 100 coral samples collected from 14 different coral species in the central Red Sea. The viral sequence portion shows that coral species significantly differ from each other, but the most abundant viral families were consistently present. Notably, we found a pervasive abundance of Baculoviridae in metagenomes. In contrast, Polydnaviridae were the most abundant viruses in metatranscriptomes, highlighting that the combined approach of metagenomics and metatranscriptomics is informative with regard to deciphering viral diversity and activity. Our study provides a first comprehensive description of viruses associated with Red Sea corals. In line with previous studies, we confirm the presence of Baculoviridae, Polydnaviridae, Phycodnaviridae, Mimiviridae, and Herpesviridae, which may be considered viral families that are globally and commonly associated with corals. The reason for the pervasive abundance of Baculoviridae in Red Sea corals at present remains unknown, but it is tempting to speculate that the association is related to the uniquely warm and salty environment of the Red Sea.

Insetos são os organismos multicelulares mais bem-sucedidos no ecossistema terrestre e sua riqueza se deve, em parte, à simbiose com microrganismos. Geradora de diversidade fenotípica, a comunidade microbiana associada a insetos permite a manutenção de fenótipos complexos capazes de colonizar novos nichos e de se adaptar a fatores de estresse. A relevância da relação de simbiose na ordem Lepidoptera, todavia, tem sido questionada em função da alta variabilidade da comunidade bacteriana associada aos seus representantes. Tendo como modelo de estudo lagartas do gênero Spodoptera (Lepidoptera: Noctuidae), esse trabalho teve por objetivo melhor compreender a composição e diversidade da microbiota associada ao intestino de lepidópteros, assim como verificar o efeito da pressão de seleção direcionada à resistência na sua estrutura e capacidade de utilização de inseticidas como fonte de carbono. Para isso, foi realizada a análise metagenômica da comunidade microbiana intestinal de quatro espécies do gênero Spodoptera assim como de cinco populações naturais de S. frugiperda e de linhagens suscetível e resistentes desse inseto praga. Foram avaliadas linhagens de S. frugiperda resistentes aos inseticidas spinosad, chlorpyrifos, lambda-cyhalothrin, flubendiamide, teflubenzuron e à toxina de Bacillus thuringiensis Cry1A.105+Cry2Ab2. A análise da composição, riqueza e capacidade da comunidade bacteriana utilizar inseticidas foi baseada na determinação de índices de diversidade alfa e beta, no isolamento de bactérias intestinais em meio seletivo e na análise do potencial de crescimento dos isolados em inúmeros inseticidas. Nossos resultados indicam a importância da microbiota intestinal para esse gênero de Lepidoptera. Bactérias do gênero Enterococcus foram predominantes em todas as populações de Spodoptera analisadas, independentemente da espécie, dieta ou pressões de seleção às quais as lagartas foram expostas. Populações naturais de S. frugiperda apresentaram um microbioma mais diverso e com maior número de bactérias capazes de metabolizar inseticidas. A diversidade do microbioma, assim como a presença e capacidade de bactérias utilizarem inseticidas como fonte de carbono para o seu crescimento foram influenciadas pelo nível de exposição a tais compostos, demonstrando que, assim como o hospedeiro, a microbiota intestinal também se encontra em pressão de seleção direcionada a resistência. / Insects are the most successful multicellular organisms in the terrestrial ecosystem and their richness is partially due to symbiosis with microorganisms. The microbial community associated with insects allows the maintenance of complex phenotypes capable of colonizing new niches and adapting to stressors. The relevance of symbiosis in Lepidoptera, however, has been questioned due to the high variability of the bacterial community associated with its representatives. Using Spodoptera larvae as a model, this work aimed to better understand the composition and diversity of the gut microbiota associated with Lepidoptera, as well as to verify the effects of the selection pressure with insecticides in the microbial gut structure and the ability of members of the community to metabolize insecticides as carbon source. Thus, we performed a metagenomic analysis of the gut microbial community of four species of the genus Spodoptera (Lepidoptera: Noctuidae), as well as for five natural populations of S. frugiperda and susceptible and resistant strains of this pest. Strains of S. frugiperda resistant to the insecticides spinosad, chlorpyrifos, lambda-cyhalothrin, flubendiamide, teflubenzuron and Bacillus thuringiensis toxin Cry1A.105 + Cry2Ab2 were evaluated. The analysis of the composition, richness and ability of the bacterial community to metabolize insecticides were carried out through alpha and beta diversity indexes, isolation of intestinal bacteria in selective medium and analysis of the growth potential of isolates in multiple insecticides. Our data indicate the importance of symbiosis for S. frugiperda. Enterococcus prevailed in all populations analyzed, regardless of the species of Spodoptera, food source or selection pressure that the larvae were exposed. Microbial diversity and ability to metabolize insecticides were higher in natural populations exposed to a range of stressors in the field. The diversity of the gut microbial community associated to Spodoptera frugiperda, as well as the ability of its members to metabolize insecticides, were influenced by the degree of exposure to insecticides, showing that, like the host, the gut microbiota is also under selection pressure to resistance.

Coral reef environments have been degrading steadily over the last few decades. It is generally accepted now that coral reefs are one of the first marine ecosystems to show measurable perturbations driven by global warming. Some of theses perturbations are consequence of extreme stochastic disturbances like hurricanes or extreme thermal anomalies and therefore, can be easily identified using broad indicators like coral cover. These indicators are easy to measure and provide a general description of the system in question. The detection and interpretation of more subtle perturbation in coral communities is more complicated, both logistically and conceptually. However, detecting chronic perturbations at an early stage can increase significantly the success of early mitigating management strategies. This thesis focuses on the development and application of highly sensitive indicators that can detect subtle perturbations in coral communities. It also studies the ecological interpretation of mild perturbations and their effect on the future structure of coral reef environments. The mild thermal disturbance experienced by the Heron Island reef in the south of the Great Barrier Reef during the 2005-2006 summer, and an environmental gradient along the central coast of Venezuela (south Caribbean Sea), were used as models to test the sensitivity of coral reefs to mild disturbances at different organisation levels (organism, population, and community). At the organismal level my results showed that the intensity of bleaching that a colony shows during a mild thermal disturbance is affected by the morphology of the colony as well as the substrates surrounding the colony. Colonies surrounded by sand bleached more than colonies surrounded by dead coral or rubble. I propose that reef specific information on the relative cover of sand, rubble, and dead coral can improve the fine scale accuracy of bleaching predicting models. Studying the same mild thermal disturbance at Heron Island, I showed how demographic parameters of some populations are more sensitive to mild thermal disturbances than coral cover (the most widely used response variable in coral monitoring programs around the world). Furthermore, my results suggest that the response of coral populations to mild thermal disturbance is different in nature and intensity to the respond observed during extreme thermal disturbances. Some taxa like Stylophora pistillata, are highly sensitive to extreme thermal disturbances, and tend to be the first to die under these conditions. In contrast, this taxon was extremely tolerant to the mild thermal disturbance of early 2006 in comparison to other taxa identified previously as more tolerant than S. pistillata. This difference in the response of coral environments to milder more common disturbances can have great influence in the trajectory that coral reefs follow in a rapidly changing world. Finally at a community level, I demonstrated how the power to detect the effect of environmental conditions on coral environments is drastically increased when the coral host-endosymbiotic algae relationship is interpreted holistically. The percentage of the variability of the community structure that can be explained by environmental variables in the central coast of Venezuela is doubled when the unit of selection considered is the holobiont instead of the coral host or the endosymbiont independently. This approach can be crucial for the detection of subtle changes in coral communities as the frequency and intensity of disturbances increase rapidly. The increase in detection power provided by the different approaches developed in this project can both improve our understanding of the structuring role of mild disturbances in coral communities as well as help identify the effect of disturbances in an early stage before the perturbation reaches catastrophic proportions. This early identification of perturbations can be used for the development of adaptive management strategies that can increase the resistance and resilience of coral reefs in the future.

As climate change intensifies, the capacity of organisms to adapt to changing environments becomes increasingly relevant. Heat-induced coral bleaching –the breakdown of the symbiotic association between coral hosts and photosynthetic algae of the family Symbiodiniaceae– is rapidly degrading reefs worldwide. Hence, there is a growing interest to study symbioses that can persist in extreme conditions. The Red Sea is such a place, known as one of the hottest seas where healthy coral reef systems thrive. Here (Chapter 1), we tested the potential of symbiont manipulation as means to improve the thermal resilience of the cnidarian holobiont, particularly using heat tolerant symbiont species from the Red Sea. We used clonal lineages of the model system Aiptasia (host and symbiont), originating from different thermal environments to assess how interchanging either partner affected their short- and long-term performance under heat stress. Our findings revealed that symbioses are not only intra-specific but have also adapted to native, local environments, thus potentially limiting the acclimation capacity of symbiotic cnidarians to climate change. As such, infection with more heat resistant species, even if native, might not necessarily improve thermotolerance of the holobiont. We further investigated (Chapter 2) how environment-dependent specificity, in this case elevated temperature, affects the establishment of novel symbioses. That is, if Aiptasia hosts are, despite exhibiting a high degree of partner fidelity, capable of acquiring more thermotolerant symbionts under stress conditions. Thus, we examined the infection dynamics of multi-species symbioses under different thermal environments and assessed their performance to subsequent heat stress. We showed that temperature, more than host identity, plays a critical role in symbiont uptake and overall performance when heatchallenged. Additionally, we found that pre-exposure to high temperature plays a fundamental role in improving the response to thermal stress, yet, this can be heavily influenced by other factors like feeding. Like climate change, ocean acidification is a serious threat to corals. Yet, most research has focused on the host and little is known for the algal partner. Thus, here we studied (Chapter 3) the global transcriptomic response of an endosymbiotic dinoflagellate to long-term seawater acidification stress. Our results revealed that despite observing an enrichment of processes related to photosynthesis and carbon fixation, which might seem beneficial to the symbiont, low pH has a detrimental effect on its photo-physiology. Taken together, this dissertation provides valuable insights into the responses of symbiotic cnidarians to future climate and ocean changes.

Ces travaux de thèse reposent sur le double objectif de proposer des approches innovantes pour l’étude des relations entre un hôte et son microbiote, et de les appliquer à la description fine de l’holobionte du puceron du pois par des données métagénomiques. Les relations symbiotiques façonnent le fonctionnement et l’évolution de tous les organismes, mais restent décrites de manière imparfaite, notamment à cause de la difficulté à caractériser la diversité génomique des partenaires microbiens constitutifs des holobiontes. L’essor des technologies de séquençage métagénomique révolutionne l’étude de ces systèmes, mais pose également des problèmes méthodologiques pour analyser les jeux de données métagénomiques. La métagénomique est ici appliquée au puceron du pois, un modèle d’étude des relations symbiotiques qui abrite une communauté bactérienne d’une complexité modérée, idéale pour développer de nouvelles approches de caractérisation de la diversité microbienne. Cette thèse vise à mieux décrire la communauté de symbiotes qu’abrite cet holobionte, notamment en distinguant les différents niveaux de variabilité génomique en son sein. Nous présentons une démarche pour l’analyse métagénomique d’holobiontes, qui repose d’abord sur l’assignation taxonomiques des lectures par alignement à des génomes de référence ou préalablement assemblés, puis sur la recherche de variants génomiques. L’étude de génotypes complets de symbiotes permet de retracer l’histoire évolutive des relations hôte-microbiote avec une résolution élevée. Chez le puceron du pois, nous mettons en évidence des niveaux et structures de diversité génomique différents selon les symbiotes, que nous proposons d’expliquer par les modalités de transmission ou l’histoire évolutive propre à chacun des partenaires microbiens. Cette approche repose sur la disponibilité d’un génome de référence adapté, qui est souvent difficile à obtenir en métagénomique. Dans un second temps, nous présentons donc une méthode d’assemblage guidé par référence en contexte métagénomique. Cette méthode se déroule en deux temps : le recrutement et l’assemblage de lectures par alignement sur un génome de référence distant, puis l’assemblage de novo ciblé des régions manquantes, permis par des développements complémentaires apportés au logiciel MindTheGap. Comparativement à un assembleur métagénomique, cette méthode permet l’assemblage d’un seul génome en un temps réduit, et permet de détecter d’éventuels variants structuraux sur le génome ciblé. Appliqué au puceron du pois, MindTheGap a réalisé l’assemblage du symbiote obligatoire Buchnera en un seul contig, et a permis d’identifier différents variants structuraux du bactériophage APSE. Ces travaux ouvrent la voie à la fois à une caractérisation plus précise des relations hôte-microbiote chez le puceron du pois par des approches fonctionnelles et métaboliques, ainsi qu’à l’application des outils présentés à des systèmes plus complexes. / The aim of this PhD thesis is to develop innovative approaches to characterize host-microbiota relationships, and to apply them to finely explore the pea aphid microbiota using metagenomic data. Symbiotic relationships play a major role in the life and evolution of all organisms, but are imperfectly described, essentially because of the difficult characterization of the genomic diversity of the microbial partners. The rise of high throughput metagenomic sequencing is a game changer for the study of those systems, but also raises methodological issues to analyze large metagenomic datasets. Metagenomic is here applied to the pea aphid holobiont, a model system for the study of symbiotic relationships, sheltering a moderately complex microbial community. This level of complexity seems to be ideal to develop new approaches for the strain-resolved characterization of host-microbiota relationships. This thesis aims at a better description of this symbiotic community by distinguishing several scales of metagenomic diversity. In a first part, we present a framework for the metagenomic analysis of holobionts, relying first on the taxonomic assignation of reads by alignment to reference or newly assembled genomes, and then on the detection of genomic variants. Whole genome variant profiles make possible to track the evolutionary history of host-microbiota associations with a high resolution. In the case of the pea aphid, we highlight different scales and structures for the metagenomic diversity of the different symbionts, accounting for different transmission modes or evolutionary histories specific to each microbial partner. This framework is based on the availability of a suitable reference genome, that may be hard to obtain in a metagenomic context. In a second part, we therefore present a novel method for reference guided genome assembly from metagenomic data. This method is based on two steps. First, the recruitment and assembly of reads by mapping metagenomic reads on a distant reference genome, and second, the de novo assembly of the missing regions, allowed by the development of an improved version of the software MindTheGap. Compared to a standard metagenomic assembler, this methods makes possible to assemble a single genome in a reasonable time, and allows to detect eventual structural variations within the targeted genome. When applied to the pea aphid holobiont, MindTheGap yielded single contig assemblie of the obligatory symbiont Buchnera aphidicola, and helped to identify different structural variants of the bacteriophage APSE. This works paves the way to a finer characterization of host-microbiota interactions, and to the application of the presented approaches to more complex systems.

Coral bleaching, i.e. the loss of photosynthetic algal symbionts, caused by ocean warming is now the main factor driving reef decline, but not all corals are affected equally. Corals from the Arabian Seas have unusually high temperature tolerances, and recently studies implicated salinity as one of the contributing factors. In particular, a recent heat stress experiment at different salinities using the model system Aiptasia and Red Sea corals, showed that cnidaria at large bleach less at heat stress under high salinities and that this is associated with an increase of the osmolyte, floridoside Here we were interested to assess microbial community changes under heat stress at different salinity levels and whether this could help to explain the increase in thermal tolerance of the metaorganism at high salinities. We determined microbial community composition via HiSeq 16S rRNA gene amplicon sequencing of two anemone strains that differ in their associated symbionts, namely H2-SSB01 (type B1) and CC7-SSA01 (type A4), after six days under ambient (25 °C) and heat stress (34 °C) temperatures at salinities of 36, 39, and 42. Both anemones harbored distinct microbial communities, irrespective of temperature or salinity, that were also different from the bacteria in surrounding seawater. Within both host-endosymbiont pairings, the bacterial community composition at low (36) and intermediate (39) salinities did not differ between ambient and heat stress, but was significantly different at high (42) salinities. Subsequent elucidation of bacterial indicator species revealed several taxa that could be associated with a response to temperature and salinity. Our results underline that microbial community composition adjusts under different environmental settings. Importantly, microbial community dynamics of H2-SSB01 aligned with observed differences in bleaching susceptibility and thermal tolerance, whereas the pattern remains unclear for CC7-SSA01, which harbors an intrinsically higher thermal tolerance. Such responses could argue for a contribution of the microbiome to the observed increase in temperature tolerance of the Aiptasia metaorganism at increased salinities. An alternative interpretation is that the microbiome changes denotes a parallel response to changing salinities.

No description available.

Microorganisms provide essential services for host organisms and this is especially true for communities of algal symbionts and bacteria hosted by tropical reef-building corals–collectively termed the coral holobiont. Endosymbiotic algae provide essential nutrients to the host, and can impact coral growth and susceptibility to environmental stress. Corals also associate with a diverse microbiome, and specific bacterial taxa have been implicated in important nutritional and immunity roles. However, fundamental questions regarding the environmental factors that govern coral holobiont composition remain unanswered. The overarching goal of my dissertation is to characterize how environmental variation, including disturbance, influences the composition of coral-associated algal and bacterial communities. To achieve this goal, I first compared these communities across reef zones (locales differing in diel thermal variability and other factors) in tandem with host genetic background under baseline conditions. I found that in the more stable reef zone, algal communities were more diverse and that host genetic diversity correlated with bacterial diversity, implying the more variable reef zone constrained diversity of host-microbial partnerships. Next, I characterized how these communities responded to a hurricane disturbance in two stress-tolerant congeneric coral species. Again, I observed stark differences across reef zones in algal symbiont and bacterial communities, but these communities were not exceptionally impacted by disturbance. Finally, I experimentally tested the role of daily thermal variability as a key environmental factor in shaping holobiont community composition and heat tolerance. While thermal variation treatment increased algal photosynthetic efficiency, it did not facilitate coral thermal tolerance to heat stress. Specific bacterial taxa were differentially abundant after 90 days in treatment acclimation, suggesting that thermal variation may contribute to part of the observed community differences across natural reef zones. In sum, this dissertation provides a deeper understanding of the interplay between coral-associated microorganisms and their local reef environments, as well as taxa-specific patterns of interest for monitoring coral holobiont dynamics under rapidly changing oceans.

Les plantes vivent en association avec une grande diversité de microorganismes qui forment son microbiota. Ce microbiote fournit des fonctions clés qui influencent tous les aspects de la vie d'une plante, de l'établissement à la croissance jusqu'à la production. Cette thèse a pour intention de déterminer les règlent d'assemblage du microbiote et ses conséquences pour le phénotypel l'adaptation et l'évolution des plantes. Pour atteindre cet objectif nous avont utilisé différentes approches expérimentales comprenant des plantes clonales comme organismes modèles ainsi que des mésocosmes prairiaux pour analyses à l'échelle des communautés. Nos résultats ont démontré i) que les Champignons Mycohiziens à Arbuscules induisent d'important es variations phénotypiques pour les traits des plantes clonales impliqués dans l'exploration de l'espace et l'exploitation des ressources. Ces changements dépendent de l'identité des symbiontes et altèrent les capacités des plantes à développer des réponses plastiques à l'hétérogénéité environnementale. ii) Les plantes ont évolué un méchanisme permettant la transmission d'une partie de leur microbiote a leur descendance, assurant la qualité de leur habitat. iii) Le contexte spécifique des communautés de plantes est un facteur majeur structurant l'assemblage du microbiota des plantes à échelle locale. L'abondance de certaines espèces de plante dans le voisinage d'une plante cible augmente ou diminue la diversité de son microbiote, déterminant in fine ses performances. De manière générale, cette thèse démontre l'importance des organismes symbiotiques dans la compréhension de l'adaptation et de l'évolution des plantes. / Plants live in association with a wide diversity of microorganisms forming the microbiota. The plant microbiota provides a variety of key functions that influence many aspects of plant's life comprising establishment, growth and reproduction. The present thesis aims at determining the assembly rules of the plant microbiota and its consequences for plant phenotype, adaptation and evolution. To fulfill this objective, we used different experimental approaches using either clonal plants as model organisms or grassland mesocosms for community-wide analyses. Our results demonstrated i) that Arbuscular Mycorrhizal Fungi induce important phenotypic variations in clonal plants traits involved in space exploration and resources exploitation. These changes depended on the identity of the symbionts and altered the plants ability to produce plastic responses to environmental heterogeneity. ii) Plants have evolved a mechanism allowing the transmission of a part of their microbiota to their progeny, ensuring thus their habitat quality. iii) The plant community context is a major factor structuring local plant microbiota assembly. Particular plant species identity in the neighborhood increase or decrease the microbiota diversity and ultimately determine the focal plant performance. This thesis overall demonstrates the importance of symbiotic microorganisms in the understanding of the plant adaptation and evolution. From the knowledges acquired we developed a novel understanding of symbiotic interactions in clonal plants by extending the holobiont theory to the meta-holobiont theory.

Relações de simbiose são comuns na natureza e tornaram-se fundamentais para a desconstrução do antigo conceito de indivíduo, único e indivisível, para o surgimento da ideia do holobionte, definido como o ser constituído de características próprias somadas aos simbiontes a ele associados. Tais relações são comuns em Insecta, sendo bactérias os microrganismos mais comumente encontrados em simbiose, influenciando diversos aspectos bioecológicos do hospedeiro. Dentre os insetos, pulgões são organismos modelos para o estudo de interações com simbiontes devido à associação com diversas espécies de bactérias, as quais produzem diferentes fenótipos do hospedeiro. Este trabalho teve por objetivo avaliar o papel do endossimbionte secundário Arsenophonus nas interações de seu hospedeiro Aphis citricidus (Kirkaldy) (Hemiptera: Aphididae) com o primeiro e terceiro níveis tróficos. Assim, isolinhagens de A. citricidus infectadas (Ars+) ou não (Ars-) por Arsenophonus foram estabelecidas e utilizadas para a condução de estudos comparativos para a exploração de plantas hospedeiras com diferentes valores nutricionais, Citrus sinensis (hospedeiro ótimo) e Murraya paniculata (hospedeiro subótimo). Foram observadas a sobrevivência, longevidade e fecundidade de A. citricidus Ars+ e Ars- em cada planta hospedeira, sendo os valores obtidos utilizados na construção de tabelas de vida de fertilidade. Para o estudo das interações com o terceiro nível trófico, foram realizados estudos comparativos do parasitismo de A. citricidus Ars+ e Ars-, criados em ambos hospedeiros, pelo parasitoide Aphelinus asychis (Walker) (Hymenoptera: Aphelinidae). Foram observados o desenvolvimento do parasitoide e o sucesso de parasitismo. Os resultados obtidos comprovaram ser C. sinensis o hospedeiro mais adequado e que o simbionte secundário beneficia seu hospedeiro na exploração do alimento, resultando na redução do período de desenvolvimento e em insetos de maior tamanho no hospedeiro subótimo. Os parâmetros de tabela de vida de fertilidade calculados para pulgões Ars+ foram superiores aos de Ars-. Além de beneficiar A. citricidus na utilização do alimento, o simbionte Arsenophonus também afetou a relação de seu hospedeiro com o parasitoide A. asychis. Pulgões Ars+ foram inadequados ao completo desenvolvimento do parasitoide. A relação de simbiose de A. citricidus e Arsenophonus estudada demonstrou a importância de simbiontes secundários nas interações multitróficas do hospedeiro e as implicações que elas podem ter para o controle do crescimento populacional de insetos de interesse econômico. / Symbiotic relationships are common in nature and have become essential for the deconstruction of the old concept of individual, as a single and indivisible entity, for the emergence of the holobiont idea, being consisted of its own characteristics added to the symbionts associated with it. Such relationships are common in Insecta, and bacteria are the microorganisms most commonly found in symbiosis, influencing many bioecological aspects of the host. Among insects, aphids are model organisms for the study of interactions with symbionts due to their association with various species of bacteria that produce different host phenotypes. This study aimed to evaluate the role of the secondary endosymbiont Arsenophonus on the interactions of its host Aphis citricidus (Kirkaldy) (Hemiptera: Aphididae) with the first and third trophic levels. Thus, isofemale strains of A. citricidus infected (Ars+) or not (Ars-) with Arsenophonus were established and used to conduct comparative studies on the use of host plants with different nutritional values, Citrus sinensis (optimum host) and Murraya paniculata (suboptimum host). We assessed survival, longevity and fecundity rates of Ars- and Ars+ A. citricidus in each host plant, and the obtained data were used in for calculation of fertility life tables. We also carried out comparative studies on the success of parasitization of Ars- and Ars+ A. citricidus reared on both host plants by the parasitoid Aphelinus asychis (Walker) (Hymenoptera: Aphelinidae). We assessed parasitoid development on aphids reared on both host plants and measured the success of parasitization on aphids reared on the optimum host plant. Our data proved C. sinensis as a more suitable host than M. paniculata, and that the secondary symbiont benefited infected aphids to explore the food source by reducing the time of development and producing larger adults in the suboptimal host. The fertility life table parameters calculated for Ars+ aphids were higher than those for Ars-. Besides benefiting A. citricidus in the use of food, Arsenophonus also affected the relationship of its host with the parasitoid A. asychis. Ars+ aphids were unsuitable to A. asychis and did not allow the full development of the parasitoid. The studied symbiotic relationship of A. citricidus and Arsenophonus showed the importance of secondary symbionts in multitrophic interactions of the host and the implications they may have for controlling the population growth of insects of economic interest.